TY - JOUR AB - Elaborate sexual signals are thought to have evolved and be maintained to serve as honest indicators of signaller quality. One measure of quality is health, which can be affected by parasite infection. Cnemaspis mysoriensis is a diurnal gecko that is often infested with ectoparasites in the wild, and males of this species express visual (coloured gular patches) and chemical (femoral gland secretions) traits that receivers could assess during social interactions. In this paper, we tested whether ectoparasites affect individual health, and whether signal quality is an indicator of ectoparasite levels. In wild lizards, we found that ectoparasite level was negatively correlated with body condition in both sexes. Moreover, some characteristics of both visual and chemical traits in males were strongly associated with ectoparasite levels. Specifically, males with higher ectoparasite levels had yellow gular patches with lower brightness and chroma, and chemical secretions with a lower proportion of aromatic compounds. We then determined whether ectoparasite levels in males influence female behaviour. Using sequential choice trials, wherein females were provided with either the visual or the chemical signals of wild-caught males that varied in ectoparasite level, we found that only chemical secretions evoked an elevated female response towards less parasitised males. Simultaneous choice trials in which females were exposed to the chemical secretions from males that varied in parasite level further confirmed a preference for males with lower parasites loads. Overall, we find that although health (body condition) or ectoparasite load can be honestly advertised through multiple modalities, the parasite-mediated female response is exclusively driven by chemical signals. AU - Pal, Arka AU - Joshi, Mihir AU - Thaker, Maria ID - 14850 IS - 1 JF - Journal of Experimental Biology KW - Insect Science KW - Molecular Biology KW - Animal Science and Zoology KW - Aquatic Science KW - Physiology KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 1477-9145 TI - Too much information? Males convey parasite levels using more signal modalities than females utilise VL - 227 ER - TY - THES AB - In nature, different species find their niche in a range of environments, each with its unique characteristics. While some thrive in uniform (homogeneous) landscapes where environmental conditions stay relatively consistent across space, others traverse the complexities of spatially heterogeneous terrains. Comprehending how species are distributed and how they interact within these landscapes holds the key to gaining insights into their evolutionary dynamics while also informing conservation and management strategies. For species inhabiting heterogeneous landscapes, when the rate of dispersal is low compared to spatial fluctuations in selection pressure, localized adaptations may emerge. Such adaptation in response to varying selection strengths plays an important role in the persistence of populations in our rapidly changing world. Hence, species in nature are continuously in a struggle to adapt to local environmental conditions, to ensure their continued survival. Natural populations can often adapt in time scales short enough for evolutionary changes to influence ecological dynamics and vice versa, thereby creating a feedback between evolution and demography. The analysis of this feedback and the relative contributions of gene flow, demography, drift, and natural selection to genetic variation and differentiation has remained a recurring theme in evolutionary biology. Nevertheless, the effective role of these forces in maintaining variation and shaping patterns of diversity is not fully understood. Even in homogeneous environments devoid of local adaptations, such understanding remains elusive. Understanding this feedback is crucial, for example in determining the conditions under which extinction risk can be mitigated in peripheral populations subject to deleterious mutation accumulation at the edges of species’ ranges as well as in highly fragmented populations. In this thesis we explore both uniform and spatially heterogeneous metapopulations, investigating and providing theoretical insights into the dynamics of local adaptation in the latter and examining the dynamics of load and extinction as well as the impact of joint ecological and evolutionary (eco-evolutionary) dynamics in the former. The thesis is divided into 5 chapters. Chapter 1 provides a general introduction into the subject matter, clarifying concepts and ideas used throughout the thesis. In chapter 2, we explore how fast a species distributed across a heterogeneous landscape adapts to changing conditions marked by alterations in carrying capacity, selection pressure, and migration rate. In chapter 3, we investigate how migration selection and drift influences adaptation and the maintenance of variation in a metapopulation with three habitats, an extension of previous models of adaptation in two habitats. We further develop analytical approximations for the critical threshold required for polymorphism to persist. The focus of chapter 4 of the thesis is on understanding the interplay between ecology and evolution as coupled processes. We investigate how eco-evolutionary feedback between migration, selection, drift, and demography influences eco-evolutionary outcomes in marginal populations subject to deleterious mutation accumulation. Using simulations as well as theoretical approximations of the coupled dynamics of population size and allele frequency, we analyze how gene flow from a large mainland source influences genetic load and population size on an island (i.e., in a marginal population) under genetically realistic assumptions. Analyses of this sort are important because small isolated populations, are repeatedly affected by complex interactions between ecological and evolutionary processes, which can lead to their death. Understanding these interactions can therefore provide an insight into the conditions under which extinction risk can be mitigated in peripheral populations thus, contributing to conservation and restoration efforts. Chapter 5 extends the analysis in chapter 4 to consider the dynamics of load (due to deleterious mutation accumulation) and extinction risk in a metapopulation. We explore the role of gene flow, selection, and dominance on load and extinction risk and further pinpoint critical thresholds required for metapopulation persistence. Overall this research contributes to our understanding of ecological and evolutionary mechanisms that shape species’ persistence in fragmented landscapes, a crucial foundation for successful conservation efforts and biodiversity management. AU - Olusanya, Oluwafunmilola O ID - 14711 SN - 2663 - 337X TI - Local adaptation, genetic load and extinction in metapopulations ER - TY - JOUR AB - Key innovations are fundamental to biological diversification, but their genetic basis is poorly understood. A recent transition from egg-laying to live-bearing in marine snails (Littorina spp.) provides the opportunity to study the genetic architecture of an innovation that has evolved repeatedly across animals. Individuals do not cluster by reproductive mode in a genome-wide phylogeny, but local genealogical analysis revealed numerous small genomic regions where all live-bearers carry the same core haplotype. Candidate regions show evidence for live-bearer–specific positive selection and are enriched for genes that are differentially expressed between egg-laying and live-bearing reproductive systems. Ages of selective sweeps suggest that live-bearer–specific alleles accumulated over more than 200,000 generations. Our results suggest that new functions evolve through the recruitment of many alleles rather than in a single evolutionary step. AU - Stankowski, Sean AU - Zagrodzka, Zuzanna B. AU - Garlovsky, Martin D. AU - Pal, Arka AU - Shipilina, Daria AU - Garcia Castillo, Diego Fernando AU - Lifchitz, Hila AU - Le Moan, Alan AU - Leder, Erica AU - Reeve, James AU - Johannesson, Kerstin AU - Westram, Anja M AU - Butlin, Roger K. ID - 14796 IS - 6678 JF - Science TI - The genetic basis of a recent transition to live-bearing in marine snails VL - 383 ER - TY - THES AB - This thesis consists of four distinct pieces of work within theoretical biology, with two themes in common: the concept of optimization in biological systems, and the use of information-theoretic tools to quantify biological stochasticity and statistical uncertainty. Chapter 2 develops a statistical framework for studying biological systems which we believe to be optimized for a particular utility function, such as retinal neurons conveying information about visual stimuli. We formalize such beliefs as maximum-entropy Bayesian priors, constrained by the expected utility. We explore how such priors aid inference of system parameters with limited data and enable optimality hypothesis testing: is the utility higher than by chance? Chapter 3 examines the ultimate biological optimization process: evolution by natural selection. As some individuals survive and reproduce more successfully than others, populations evolve towards fitter genotypes and phenotypes. We formalize this as accumulation of genetic information, and use population genetics theory to study how much such information can be accumulated per generation and maintained in the face of random mutation and genetic drift. We identify the population size and fitness variance as the key quantities that control information accumulation and maintenance. Chapter 4 reuses the concept of genetic information from Chapter 3, but from a different perspective: we ask how much genetic information organisms actually need, in particular in the context of gene regulation. For example, how much information is needed to bind transcription factors at correct locations within the genome? Population genetics provides us with a refined answer: with an increasing population size, populations achieve higher fitness by maintaining more genetic information. Moreover, regulatory parameters experience selection pressure to optimize the fitness-information trade-off, i.e. minimize the information needed for a given fitness. This provides an evolutionary derivation of the optimization priors introduced in Chapter 2. Chapter 5 proves an upper bound on mutual information between a signal and a communication channel output (such as neural activity). Mutual information is an important utility measure for biological systems, but its practical use can be difficult due to the large dimensionality of many biological channels. Sometimes, a lower bound on mutual information is computed by replacing the high-dimensional channel outputs with decodes (signal estimates). Our result provides a corresponding upper bound, provided that the decodes are the maximum posterior estimates of the signal. AU - Hledik, Michal ID - 15020 KW - Theoretical biology KW - Optimality KW - Evolution KW - Information SN - 2663 - 337X TI - Genetic information and biological optimization ER - TY - JOUR AB - Speciation is a key evolutionary process that is not yet fully understood. Combining population genomic and ecological data from multiple diverging pairs of marine snails (Littorina) supports the search for speciation mechanisms. Placing pairs on a one-dimensional speciation continuum, from undifferentiated populations to species, obscured the complexity of speciation. Adding multiple axes helped to describe either speciation routes or reproductive isolation in the snails. Divergent ecological selection repeatedly generated barriers between ecotypes, but appeared less important in completing speciation while genetic incompatibilities played a key role. Chromosomal inversions contributed to genomic barriers, but with variable impact. A multidimensional (hypercube) approach supported framing of questions and identification of knowledge gaps and can be useful to understand speciation in many other systems. AU - Johannesson, Kerstin AU - Faria, Rui AU - Le Moan, Alan AU - Rafajlović, Marina AU - Westram, Anja M AU - Butlin, Roger K. AU - Stankowski, Sean ID - 15099 JF - Trends in Genetics SN - 0168-9525 TI - Diverse pathways to speciation revealed by marine snails ER - TY - JOUR AB - Understanding population divergence that eventually leads to speciation is essential for evolutionary biology. High species diversity in the sea was regarded as a paradox when strict allopatry was considered necessary for most speciation events because geographical barriers seemed largely absent in the sea, and many marine species have high dispersal capacities. Combining genome-wide data with demographic modelling to infer the demographic history of divergence has introduced new ways to address this classical issue. These models assume an ancestral population that splits into two subpopulations diverging according to different scenarios that allow tests for periods of gene flow. Models can also test for heterogeneities in population sizes and migration rates along the genome to account, respectively, for background selection and selection against introgressed ancestry. To investigate how barriers to gene flow arise in the sea, we compiled studies modelling the demographic history of divergence in marine organisms and extracted preferred demographic scenarios together with estimates of demographic parameters. These studies show that geographical barriers to gene flow do exist in the sea but that divergence can also occur without strict isolation. Heterogeneity of gene flow was detected in most population pairs suggesting the predominance of semipermeable barriers during divergence. We found a weak positive relationship between the fraction of the genome experiencing reduced gene flow and levels of genome-wide differentiation. Furthermore, we found that the upper bound of the ‘grey zone of speciation’ for our dataset extended beyond that found before, implying that gene flow between diverging taxa is possible at higher levels of divergence than previously thought. Finally, we list recommendations for further strengthening the use of demographic modelling in speciation research. These include a more balanced representation of taxa, more consistent and comprehensive modelling, clear reporting of results and simulation studies to rule out nonbiological explanations for general results. AU - De Jode, Aurélien AU - Le Moan, Alan AU - Johannesson, Kerstin AU - Faria, Rui AU - Stankowski, Sean AU - Westram, Anja M AU - Butlin, Roger K. AU - Rafajlović, Marina AU - Fraisse, Christelle ID - 11479 IS - 2 JF - Evolutionary Applications TI - Ten years of demographic modelling of divergence and speciation in the sea VL - 16 ER - TY - JOUR AB - The concept of a “speciation continuum” has gained popularity in recent decades. It emphasizes speciation as a continuous process that may be studied by comparing contemporary population pairs that show differing levels of divergence. In their recent perspective article in Evolution, Stankowski and Ravinet provided a valuable service by formally defining the speciation continuum as a continuum of reproductive isolation, based on opinions gathered from a survey of speciation researchers. While we agree that the speciation continuum has been a useful concept to advance the understanding of the speciation process, some intrinsic limitations exist. Here, we advocate for a multivariate extension, the speciation hypercube, first proposed by Dieckmann et al. in 2004, but rarely used since. We extend the idea of the speciation cube and suggest it has strong conceptual and practical advantages over a one-dimensional model. We illustrate how the speciation hypercube can be used to visualize and compare different speciation trajectories, providing new insights into the processes and mechanisms of speciation. A key strength of the speciation hypercube is that it provides a unifying framework for speciation research, as it allows questions from apparently disparate subfields to be addressed in a single conceptual model. AU - Bolnick, Daniel I. AU - Hund, Amanda K. AU - Nosil, Patrik AU - Peng, Foen AU - Ravinet, Mark AU - Stankowski, Sean AU - Subramanian, Swapna AU - Wolf, Jochen B.W. AU - Yukilevich, Roman ID - 12514 IS - 1 JF - Evolution: International journal of organic evolution TI - A multivariate view of the speciation continuum VL - 77 ER - TY - JOUR AB - The term “haplotype block” is commonly used in the developing field of haplotype-based inference methods. We argue that the term should be defined based on the structure of the Ancestral Recombination Graph (ARG), which contains complete information on the ancestry of a sample. We use simulated examples to demonstrate key features of the relationship between haplotype blocks and ancestral structure, emphasizing the stochasticity of the processes that generate them. Even the simplest cases of neutrality or of a “hard” selective sweep produce a rich structure, often missed by commonly used statistics. We highlight a number of novel methods for inferring haplotype structure, based on the full ARG, or on a sequence of trees, and illustrate how they can be used to define haplotype blocks using an empirical data set. While the advent of new, computationally efficient methods makes it possible to apply these concepts broadly, they (and additional new methods) could benefit from adding features to explore haplotype blocks, as we define them. Understanding and applying the concept of the haplotype block will be essential to fully exploit long and linked-read sequencing technologies. AU - Shipilina, Daria AU - Pal, Arka AU - Stankowski, Sean AU - Chan, Yingguang Frank AU - Barton, Nicholas H ID - 12159 IS - 6 JF - Molecular Ecology KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0962-1083 TI - On the origin and structure of haplotype blocks VL - 32 ER - TY - JOUR AB - The classical infinitesimal model is a simple and robust model for the inheritance of quantitative traits. In this model, a quantitative trait is expressed as the sum of a genetic and an environmental component, and the genetic component of offspring traits within a family follows a normal distribution around the average of the parents’ trait values, and has a variance that is independent of the parental traits. In previous work, we showed that when trait values are determined by the sum of a large number of additive Mendelian factors, each of small effect, one can justify the infinitesimal model as a limit of Mendelian inheritance. In this paper, we show that this result extends to include dominance. We define the model in terms of classical quantities of quantitative genetics, before justifying it as a limit of Mendelian inheritance as the number, M, of underlying loci tends to infinity. As in the additive case, the multivariate normal distribution of trait values across the pedigree can be expressed in terms of variance components in an ancestral population and probabilities of identity by descent determined by the pedigree. Now, with just first-order dominance effects, we require two-, three-, and four-way identities. We also show that, even if we condition on parental trait values, the “shared” and “residual” components of trait values within each family will be asymptotically normally distributed as the number of loci tends to infinity, with an error of order 1/M−−√⁠. We illustrate our results with some numerical examples. AU - Barton, Nicholas H AU - Etheridge, Alison M. AU - Véber, Amandine ID - 14452 IS - 2 JF - Genetics SN - 0016-6731 TI - The infinitesimal model with dominance VL - 225 ER - TY - DATA AB - The classical infinitesimal model is a simple and robust model for the inheritance of quantitative traits. In this model, a quantitative trait is expressed as the sum of a genetic and a non-genetic (environmental) component and the genetic component of offspring traits within a family follows a normal distribution around the average of the parents’ trait values, and has a variance that is independent of the trait values of the parents. Although the trait distribution across the whole population can be far from normal, the trait distributions within families are normally distributed with a variance-covariance matrix that is determined entirely by that in the ancestral population and the probabilities of identity determined by the pedigree. Moreover, conditioning on some of the trait values within the pedigree has predictable effects on the mean and variance within and between families. In previous work, Barton et al. (2017), we showed that when trait values are determined by the sum of a large number of Mendelian factors, each of small effect, one can justify the infinitesimal model as limit of Mendelian inheritance. It was also shown that under some forms of epistasis, trait values within a family are still normally distributed. AU - Barton, Nicholas H ID - 12949 KW - Quantitative genetics KW - infinitesimal model TI - The infinitesimal model with dominance ER - TY - JOUR AB - Inversions are structural mutations that reverse the sequence of a chromosome segment and reduce the effective rate of recombination in the heterozygous state. They play a major role in adaptation, as well as in other evolutionary processes such as speciation. Although inversions have been studied since the 1920s, they remain difficult to investigate because the reduced recombination conferred by them strengthens the effects of drift and hitchhiking, which in turn can obscure signatures of selection. Nonetheless, numerous inversions have been found to be under selection. Given recent advances in population genetic theory and empirical study, here we review how different mechanisms of selection affect the evolution of inversions. A key difference between inversions and other mutations, such as single nucleotide variants, is that the fitness of an inversion may be affected by a larger number of frequently interacting processes. This considerably complicates the analysis of the causes underlying the evolution of inversions. We discuss the extent to which these mechanisms can be disentangled, and by which approach. AU - Berdan, Emma L. AU - Barton, Nicholas H AU - Butlin, Roger AU - Charlesworth, Brian AU - Faria, Rui AU - Fragata, Inês AU - Gilbert, Kimberly J. AU - Jay, Paul AU - Kapun, Martin AU - Lotterhos, Katie E. AU - Mérot, Claire AU - Durmaz Mitchell, Esra AU - Pascual, Marta AU - Peichel, Catherine L. AU - Rafajlović, Marina AU - Westram, Anja M AU - Schaeffer, Stephen W. AU - Johannesson, Kerstin AU - Flatt, Thomas ID - 14556 JF - Journal of Evolutionary Biology SN - 1010-061X TI - How chromosomal inversions reorient the evolutionary process ER - TY - JOUR AB - Interactions between plants and herbivores are central in most ecosystems, but their strength is highly variable. The amount of variability within a system is thought to influence most aspects of plant-herbivore biology, from ecological stability to plant defense evolution. Our understanding of what influences variability, however, is limited by sparse data. We collected standardized surveys of herbivory for 503 plant species at 790 sites across 116° of latitude. With these data, we show that within-population variability in herbivory increases with latitude, decreases with plant size, and is phylogenetically structured. Differences in the magnitude of variability are thus central to how plant-herbivore biology varies across macroscale gradients. We argue that increased focus on interaction variability will advance understanding of patterns of life on Earth. AU - Robinson, M. L. AU - Hahn, P. G. AU - Inouye, B. D. AU - Underwood, N. AU - Whitehead, S. R. AU - Abbott, K. C. AU - Bruna, E. M. AU - Cacho, N. I. AU - Dyer, L. A. AU - Abdala-Roberts, L. AU - Allen, W. J. AU - Andrade, J. F. AU - Angulo, D. F. AU - Anjos, D. AU - Anstett, D. N. AU - Bagchi, R. AU - Bagchi, S. AU - Barbosa, M. AU - Barrett, S. AU - Baskett, Carina AU - Ben-Simchon, E. AU - Bloodworth, K. J. AU - Bronstein, J. L. AU - Buckley, Y. M. AU - Burghardt, K. T. AU - Bustos-Segura, C. AU - Calixto, E. S. AU - Carvalho, R. L. AU - Castagneyrol, B. AU - Chiuffo, M. C. AU - Cinoğlu, D. AU - Cinto Mejía, E. AU - Cock, M. C. AU - Cogni, R. AU - Cope, O. L. AU - Cornelissen, T. AU - Cortez, D. R. AU - Crowder, D. W. AU - Dallstream, C. AU - Dáttilo, W. AU - Davis, J. K. AU - Dimarco, R. D. AU - Dole, H. E. AU - Egbon, I. N. AU - Eisenring, M. AU - Ejomah, A. AU - Elderd, B. D. AU - Endara, M. J. AU - Eubanks, M. D. AU - Everingham, S. E. AU - Farah, K. N. AU - Farias, R. P. AU - Fernandes, A. P. AU - Fernandes, G. W. AU - Ferrante, M. AU - Finn, A. AU - Florjancic, G. A. AU - Forister, M. L. AU - Fox, Q. N. AU - Frago, E. AU - França, F. M. AU - Getman-Pickering, A. S. AU - Getman-Pickering, Z. AU - Gianoli, E. AU - Gooden, B. AU - Gossner, M. M. AU - Greig, K. A. AU - Gripenberg, S. AU - Groenteman, R. AU - Grof-Tisza, P. AU - Haack, N. AU - Hahn, L. AU - Haq, S. M. AU - Helms, A. M. AU - Hennecke, J. AU - Hermann, S. L. AU - Holeski, L. M. AU - Holm, S. AU - Hutchinson, M. C. AU - Jackson, E. E. AU - Kagiya, S. AU - Kalske, A. AU - Kalwajtys, M. AU - Karban, R. AU - Kariyat, R. AU - Keasar, T. AU - Kersch-Becker, M. F. AU - Kharouba, H. M. AU - Kim, T. N. AU - Kimuyu, D. M. AU - Kluse, J. AU - Koerner, S. E. AU - Komatsu, K. J. AU - Krishnan, S. AU - Laihonen, M. AU - Lamelas-López, L. AU - Lascaleia, M. C. AU - Lecomte, N. AU - Lehn, C. R. AU - Li, X. AU - Lindroth, R. L. AU - Lopresti, E. F. AU - Losada, M. AU - Louthan, A. M. AU - Luizzi, V. J. AU - Lynch, S. C. AU - Lynn, J. S. AU - Lyon, N. J. AU - Maia, L. F. AU - Maia, R. A. AU - Mannall, T. L. AU - Martin, B. S. AU - Massad, T. J. AU - Mccall, A. C. AU - Mcgurrin, K. AU - Merwin, A. C. AU - Mijango-Ramos, Z. AU - Mills, C. H. AU - Moles, A. T. AU - Moore, C. M. AU - Moreira, X. AU - Morrison, C. R. AU - Moshobane, M. C. AU - Muola, A. AU - Nakadai, R. AU - Nakajima, K. AU - Novais, S. AU - Ogbebor, C. O. AU - Ohsaki, H. AU - Pan, V. S. AU - Pardikes, N. A. AU - Pareja, M. AU - Parthasarathy, N. AU - Pawar, R. R. AU - Paynter, Q. AU - Pearse, I. S. AU - Penczykowski, R. M. AU - Pepi, A. A. AU - Pereira, C. C. AU - Phartyal, S. S. AU - Piper, F. I. AU - Poveda, K. AU - Pringle, E. G. AU - Puy, J. AU - Quijano, T. AU - Quintero, C. AU - Rasmann, S. AU - Rosche, C. AU - Rosenheim, L. Y. AU - Rosenheim, J. A. AU - Runyon, J. B. AU - Sadeh, A. AU - Sakata, Y. AU - Salcido, D. M. AU - Salgado-Luarte, C. AU - Santos, B. A. AU - Sapir, Y. AU - Sasal, Y. AU - Sato, Y. AU - Sawant, M. AU - Schroeder, H. AU - Schumann, I. AU - Segoli, M. AU - Segre, H. AU - Shelef, O. AU - Shinohara, N. AU - Singh, R. P. AU - Smith, D. S. AU - Sobral, M. AU - Stotz, G. C. AU - Tack, A. J.M. AU - Tayal, M. AU - Tooker, J. F. AU - Torrico-Bazoberry, D. AU - Tougeron, K. AU - Trowbridge, A. M. AU - Utsumi, S. AU - Uyi, O. AU - Vaca-Uribe, J. L. AU - Valtonen, A. AU - Van Dijk, L. J.A. AU - Vandvik, V. AU - Villellas, J. AU - Waller, L. P. AU - Weber, M. G. AU - Yamawo, A. AU - Yim, S. AU - Zarnetske, P. L. AU - Zehr, L. N. AU - Zhong, Z. AU - Wetzel, W. C. ID - 14552 IS - 6671 JF - Science TI - Plant size, latitude, and phylogeny explain within-population variability in herbivory VL - 382 ER - TY - GEN AB - This is associated with our paper "Plant size, latitude, and phylogeny explain within-population variability in herbivory" published in Science. AU - Wetzel, William ID - 14579 TI - HerbVar-Network/HV-Large-Patterns-MS-public: v1.0.0 ER - TY - THES AB - Females and males across species are subject to divergent selective pressures arising from di↵erent reproductive interests and ecological niches. This often translates into a intricate array of sex-specific natural and sexual selection on traits that have a shared genetic basis between both sexes, causing a genetic sexual conflict. The resolution of this conflict mostly relies on the evolution of sex-specific expression of the shared genes, leading to phenotypic sexual dimorphism. Such sex-specific gene expression is thought to evolve via modifications of the genetic networks ultimately linked to sex-determining transcription factors. Although much empirical and theoretical evidence supports this standard picture of the molecular basis of sexual conflict resolution, there still are a few open questions regarding the complex array of selective forces driving phenotypic di↵erentiation between the sexes, as well as the molecular mechanisms underlying sexspecific adaptation. I address some of these open questions in my PhD thesis. First, how do patterns of phenotypic sexual dimorphism vary within populations, as a response to the temporal and spatial changes in sex-specific selective forces? To tackle this question, I analyze the patterns of sex-specific phenotypic variation along three life stages and across populations spanning the whole geographical range of Rumex hastatulus, a wind-pollinated angiosperm, in the first Chapter of the thesis. Second, how do gene expression patterns lead to phenotypic dimorphism, and what are the molecular mechanisms underlying the observed transcriptomic variation? I address this question by examining the sex- and tissue-specific expression variation in newly-generated datasets of sex-specific expression in heads and gonads of Drosophila melanogaster. I additionally used two complementary approaches for the study of the genetic basis of sex di↵erences in gene expression in the second and third Chapters of the thesis. Third, how does intersex correlation, thought to be one of the main aspects constraining the ability for the two sexes to decouple, interact with the evolution of sexual dimorphism? I develop models of sex-specific stabilizing selection, mutation and drift to formalize common intuition regarding the patterns of covariation between intersex correlation and sexual dimorphism in the fourth Chapter of the thesis. Alltogether, the work described in this PhD thesis provides useful insights into the links between genetic, transcriptomic and phenotypic layers of sex-specific variation, and contributes to our general understanding of the dynamics of sexual dimorphism evolution. AU - Puixeu Sala, Gemma ID - 14058 SN - 2663-337X TI - The molecular basis of sexual dimorphism: Experimental and theoretical characterization of phenotypic, transcriptomic and genetic patterns of sex-specific adaptation ER - TY - JOUR AB - The regulatory architecture of gene expression is known to differ substantially between sexes in Drosophila, but most studies performed so far used whole-body data and only single crosses, which may have limited their scope to detect patterns that are robust across tissues and biological replicates. Here, we use allele-specific gene expression of parental and reciprocal hybrid crosses between 6 Drosophila melanogaster inbred lines to quantify cis- and trans-regulatory variation in heads and gonads of both sexes separately across 3 replicate crosses. Our results suggest that female and male heads, as well as ovaries, have a similar regulatory architecture. On the other hand, testes display more and substantially different cis-regulatory effects, suggesting that sex differences in the regulatory architecture that have been previously observed may largely derive from testis-specific effects. We also examine the difference in cis-regulatory variation of genes across different levels of sex bias in gonads and heads. Consistent with the idea that intersex correlations constrain expression and can lead to sexual antagonism, we find more cis variation in unbiased and moderately biased genes in heads. In ovaries, reduced cis variation is observed for male-biased genes, suggesting that cis variants acting on these genes in males do not lead to changes in ovary expression. Finally, we examine the dominance patterns of gene expression and find that sex- and tissue-specific patterns of inheritance as well as trans-regulatory variation are highly variable across biological crosses, although these were performed in highly controlled experimental conditions. This highlights the importance of using various genetic backgrounds to infer generalizable patterns. AU - Puixeu Sala, Gemma AU - Macon, Ariana AU - Vicoso, Beatriz ID - 14077 IS - 8 JF - G3: Genes, Genomes, Genetics KW - Genetics (clinical) KW - Genetics KW - Molecular Biology SN - 2160-1836 TI - Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster VL - 13 ER - TY - DATA AB - Datasets of the publication "Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster". AU - Puixeu Sala, Gemma ID - 12933 TI - Data from: Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster ER - TY - JOUR AB - Inversions are thought to play a key role in adaptation and speciation, suppressing recombination between diverging populations. Genes influencing adaptive traits cluster in inversions, and changes in inversion frequencies are associated with environmental differences. However, in many organisms, it is unclear if inversions are geographically and taxonomically widespread. The intertidal snail, Littorina saxatilis, is one such example. Strong associations between putative polymorphic inversions and phenotypic differences have been demonstrated between two ecotypes of L. saxatilis in Sweden and inferred elsewhere, but no direct evidence for inversion polymorphism currently exists across the species range. Using whole genome data from 107 snails, most inversion polymorphisms were found to be widespread across the species range. The frequencies of some inversion arrangements were significantly different among ecotypes, suggesting a parallel adaptive role. Many inversions were also polymorphic in the sister species, L. arcana, hinting at an ancient origin. AU - Reeve, James AU - Butlin, Roger K. AU - Koch, Eva L. AU - Stankowski, Sean AU - Faria, Rui ID - 14463 JF - Molecular Ecology SN - 0962-1083 TI - Chromosomal inversion polymorphisms are widespread across the species ranges of rough periwinkles (Littorina saxatilis and L. arcana) ER - TY - THES AB - For self-incompatibility (SI) to be stable in a population, theory predicts that sufficient inbreeding depression (ID) is required: the fitness of offspring from self-mated individuals must be low enough to prevent the spread of self-compatibility (SC). Reviews of natural plant populations have supported this theory, with SI species generally showing high levels of ID. However, there is thought to be an under-sampling of self-incompatible taxa in the current literature. In this thesis, I study inbreeding depression in the SI plant species Antirrhinum majus using both greenhouse crosses and a large collected field dataset. Additionally, the gametophytic S-locus of A. majus is highly heterozygous and polymorphic, thus making assembly and discovery of S-alleles very difficult. Here, 206 new alleles of the male component SLFs are presented, along with a phylogeny showing the high conservation with alleles from another Antirrhinum species. Lastly, selected sites within the protein structure of SLFs are investigated, with one site in particular highlighted as potentially being involved in the SI recognition mechanism. AU - Arathoon, Louise S ID - 14651 SN - 2663 - 337X TI - Investigating inbreeding depression and the self-incompatibility locus of Antirrhinum majus ER - TY - JOUR AB - Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life. AU - Lucek, Kay AU - Giménez, Mabel D. AU - Joron, Mathieu AU - Rafajlović, Marina AU - Searle, Jeremy B. AU - Walden, Nora AU - Westram, Anja M AU - Faria, Rui ID - 14742 IS - 11 JF - Cold Spring Harbor Perspectives in Biology KW - General Biochemistry KW - Genetics and Molecular Biology SN - 1943-0264 TI - The impact of chromosomal rearrangements in speciation: From micro- to macroevolution VL - 15 ER - TY - JOUR AB - Understanding the phenotypic and genetic architecture of reproductive isolation is a long‐standing goal of speciation research. In several systems, large‐effect loci contributing to barrier phenotypes have been characterized, but such causal connections are rarely known for more complex genetic architectures. In this study, we combine “top‐down” and “bottom‐up” approaches with demographic modelling toward an integrated understanding of speciation across a monkeyflower hybrid zone. Previous work suggests that pollinator visitation acts as a primary barrier to gene flow between two divergent red‐ and yellow‐flowered ecotypes ofMimulus aurantiacus. Several candidate isolating traits and anonymous single nucleotide polymorphism loci under divergent selection have been identified, but their genomic positions remain unknown. Here, we report findings from demographic analyses that indicate this hybrid zone formed by secondary contact, but that subsequent gene flow was restricted by widespread barrier loci across the genome. Using a novel, geographic cline‐based genome scan, we demonstrate that candidate barrier loci are broadly distributed across the genome, rather than mapping to one or a few “islands of speciation.” Quantitative trait locus (QTL) mapping reveals that most floral traits are highly polygenic, with little evidence that QTL colocalize, indicating that most traits are genetically independent. Finally, we find little evidence that QTL and candidate barrier loci overlap, suggesting that some loci contribute to other forms of reproductive isolation. Our findings highlight the challenges of understanding the genetic architecture of reproductive isolation and reveal that barriers to gene flow other than pollinator isolation may play an important role in this system. AU - Stankowski, Sean AU - Chase, Madeline A. AU - McIntosh, Hanna AU - Streisfeld, Matthew A. ID - 14787 IS - 8 JF - Molecular Ecology KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0962-1083 TI - Integrating top‐down and bottom‐up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone VL - 32 ER - TY - JOUR AB - Understanding the factors that have shaped the current distributions and diversity of species is a central and longstanding aim of evolutionary biology. The recent inclusion of genomic data into phylogeographic studies has dramatically improved our understanding in organisms where evolutionary relationships have been challenging to infer. We used whole-genome sequences to study the phylogeography of the intertidal snail Littorina saxatilis, which has successfully colonized and diversified across a broad range of coastal environments in the Northern Hemisphere amid repeated cycles of glaciation. Building on past studies based on short DNA sequences, we used genome-wide data to provide a clearer picture of the relationships among samples spanning most of the species natural range. Our results confirm the trans-Atlantic colonization of North America from Europe, and have allowed us to identify rough locations of glacial refugia and to infer likely routes of colonization within Europe. We also investigated the signals in different datasets to account for the effects of genomic architecture and non-neutral evolution, which provides new insights about diversification of four ecotypes of L. saxatilis (the crab, wave, barnacle, and brackish ecotypes) at different spatial scales. Overall, we provide a much clearer picture of the biogeography of L. saxatilis, providing a foundation for more detailed phylogenomic and demographic studies. AU - Stankowski, Sean AU - Zagrodzka, Zuzanna B AU - Galindo, Juan AU - Montaño-Rendón, Mauricio AU - Faria, Rui AU - Mikhailova, Natalia AU - Blakeslee, April M H AU - Arnason, Einar AU - Broquet, Thomas AU - Morales, Hernán E AU - Grahame, John W AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger K ID - 14833 IS - 1 JF - Evolutionary Journal of the Linnean Society TI - Whole-genome phylogeography of the intertidal snail Littorina saxatilis VL - 2 ER - TY - GEN AB - Fragmented landscapes pose a significant threat to the persistence of species as they are highly susceptible to heightened risk of extinction due to the combined effects of genetic and demographic factors such as genetic drift and demographic stochasticity. This paper explores the intricate interplay between genetic load and extinction risk within metapopulations with a focus on understanding the impact of eco-evolutionary feedback mechanisms. We distinguish between two models of selection: soft selection, characterised by subpopulations maintaining carrying capacity despite load, and hard selection, where load can significantly affect population size. Within the soft selection framework, we investigate the impact of gene flow on genetic load at a single locus, while also considering the effect of selection strength and dominance coefficient. We subsequently build on this to examine how gene flow influences both population size and load under hard selection as well as identify critical thresholds for metapopulation persistence. Our analysis employs the diffusion, semi-deterministic and effective migration approximations. Our findings reveal that under soft selection, even modest levels of migration can significantly alleviate the burden of load. In sharp contrast, with hard selection, a much higher degree of gene flow is required to mitigate load and prevent the collapse of the metapopulation. Overall, this study sheds light into the crucial role migration plays in shaping the dynamics of genetic load and extinction risk in fragmented landscapes, offering valuable insights for conservation strategies and the preservation of diversity in a changing world. AU - Olusanya, Oluwafunmilola O AU - Khudiakova, Kseniia AU - Sachdeva, Himani ID - 14732 T2 - bioRxiv TI - Genetic load, eco-evolutionary feedback and extinction in a metapopulation ER - TY - GEN AB - This repository contains the code and VCF files needed to conduct the analyses in our MS. Each folder contains a readMe document explaining the nature of each file and dataset and the results and analyses that they relate to. The same anlaysis code (but not VCF files) is also available at https://github.com/seanstankowski/Littorina_reproductive_mode AU - Stankowski, Sean ID - 14812 TI - Data and code for: The genetic architecture of a recent transition to live-bearing in marine snails ER - TY - THES AB - The evolutionary processes that brought about today’s plethora of living species and the many billions more ancient ones all underlie biology. Evolutionary pathways are neither directed nor deterministic, but rather an interplay between selection, migration, mutation, genetic drift and other environmental factors. Hybrid zones, as natural crossing experiments, offer a great opportunity to use cline analysis to deduce different evolutionary processes - for example, selection strength. Theoretical cline models, largely assuming uniform distribution of individuals, often lack the capability of incorporating population structure. Since in reality organisms mostly live in patchy distributions and their dispersal is hardly ever Gaussian, it is necessary to unravel the effect of these different elements of population structure on cline parameters and shape. In this thesis, I develop a simulation inspired by the A. majus hybrid zone of a single selected locus under frequency dependent selection. This simulation enables us to untangle the effects of different elements of population structure as for example a low-density center and long-range dispersal. This thesis is therefore a first step towards theoretically untangling the effects of different elements of population structure on cline parameters and shape. AU - Julseth, Mara ID - 12800 SN - 2791-4585 TI - The effect of local population structure on genetic variation at selected loci in the A. majus hybrid zone ER - TY - JOUR AB - When Mendel’s work was rediscovered in 1900, and extended to establish classical genetics, it was initially seen in opposition to Darwin’s theory of evolution by natural selection on continuous variation, as represented by the biometric research program that was the foundation of quantitative genetics. As Fisher, Haldane, and Wright established a century ago, Mendelian inheritance is exactly what is needed for natural selection to work efficiently. Yet, the synthesis remains unfinished. We do not understand why sexual reproduction and a fair meiosis predominate in eukaryotes, or how far these are responsible for their diversity and complexity. Moreover, although quantitative geneticists have long known that adaptive variation is highly polygenic, and that this is essential for efficient selection, this is only now becoming appreciated by molecular biologists—and we still do not have a good framework for understanding polygenic variation or diffuse function. AU - Barton, Nicholas H ID - 11702 IS - 30 JF - Proceedings of the National Academy of Sciences of the United States of America SN - 0027-8424 TI - The "New Synthesis" VL - 119 ER - TY - THES AB - Although we often see studies focusing on simple or even discrete traits in studies of colouration, the variation of “appearance” phenotypes found in nature is often more complex, continuous and high-dimensional. Therefore, we developed automated methods suitable for large datasets of genomes and images, striving to account for their complex nature, while minimising human bias. We used these methods on a dataset of more than 20, 000 plant SNP genomes and corresponding fower images from a hybrid zone of two subspecies of Antirrhinum majus with distinctly coloured fowers to improve our understanding of the genetic nature of the fower colour in our study system. Firstly, we use the advantage of large numbers of genotyped plants to estimate the haplotypes in the main fower colour regulating region. We study colour- and geography-related characteristics of the estimated haplotypes and how they connect to their relatedness. We show discrepancies from the expected fower colour distributions given the genotype and identify particular haplotypes leading to unexpected phenotypes. We also confrm a signifcant defcit of the double recessive recombinant and quite surprisingly, we show that haplotypes of the most frequent parental type are much less variable than others. Secondly, we introduce our pipeline capable of processing tens of thousands of full fower images without human interaction and summarising each image into a set of informative scores. We show the compatibility of these machine-measured fower colour scores with the previously used manual scores and study impact of external efect on the resulting scores. Finally, we use the machine-measured fower colour scores to ft and examine a phenotype cline across the hybrid zone in Planoles using full fower images as opposed to discrete, manual scores and compare it with the genotypic cline. AU - Matejovicova, Lenka ID - 11128 SN - 2663-337X TI - Genetic basis of flower colour as a model for adaptive evolution ER - TY - JOUR AB - Maternally inherited Wolbachia transinfections are being introduced into natural mosquito populations to reduce the transmission of dengue, Zika, and other arboviruses. Wolbachia-induced cytoplasmic incompatibility provides a frequency-dependent reproductive advantage to infected females that can spread transinfections within and among populations. However, because transinfections generally reduce host fitness, they tend to spread within populations only after their frequency exceeds a critical threshold. This produces bistability with stable equilibrium frequencies at both 0 and 1, analogous to the bistability produced by underdominance between alleles or karyotypes and by population dynamics under Allee effects. Here, we analyze how stochastic frequency variation produced by finite population size can facilitate the local spread of variants with bistable dynamics into areas where invasion is unexpected from deterministic models. Our exemplar is the establishment of wMel Wolbachia in the Aedes aegypti population of Pyramid Estates (PE), a small community in far north Queensland, Australia. In 2011, wMel was stably introduced into Gordonvale, separated from PE by barriers to A. aegypti dispersal. After nearly 6 years during which wMel was observed only at low frequencies in PE, corresponding to an apparent equilibrium between immigration and selection, wMel rose to fixation by 2018. Using analytic approximations and statistical analyses, we demonstrate that the observed fixation of wMel at PE is consistent with both stochastic transition past an unstable threshold frequency and deterministic transformation produced by steady immigration at a rate just above the threshold required for deterministic invasion. The indeterminacy results from a delicate balance of parameters needed to produce the delayed transition observed. Our analyses suggest that once Wolbachia transinfections are established locally through systematic introductions, stochastic “threshold crossing” is likely to only minimally enhance spatial spread, providing a local ratchet that slightly—but systematically—aids area-wide transformation of disease-vector populations in heterogeneous landscapes. AU - Turelli, Michael AU - Barton, Nicholas H ID - 10604 IS - 1 JF - Evolution Letters KW - genetics KW - ecology KW - evolution KW - behavior and systematics TI - Why did the Wolbachia transinfection cross the road? Drift, deterministic dynamics, and disease control VL - 6 ER - TY - GEN AB - Maternally inherited Wolbachia transinfections are being introduced into natural mosquito populations to reduce the transmission of dengue, Zika and other arboviruses. Wolbachia-induced cytoplasmic incompatibility provides a frequency-dependent reproductive advantage to infected females that can spread transinfections within and among populations. However, because transinfections generally reduce host fitness, they tend to spread within populations only after their frequency exceeds a critical threshold. This produces bistability with stable equilibrium frequencies at both 0 and 1, analogous to the bistability produced by underdominance between alleles or karyotypes and by population dynamics under Allee effects. Here, we analyze how stochastic frequency variation produced by finite population size can facilitate the local spread of variants with bistable dynamics into areas where invasion is unexpected from deterministic models. Our exemplar is the establishment of wMel Wolbachia in the Aedes aegypti population of Pyramid Estates (PE), a small community in far north Queensland, Australia. In 2011, wMel was stably introduced into Gordonvale, separated from PE by barriers to Ae. aegypti dispersal. After nearly six years during which wMel was observed only at low frequencies in PE, corresponding to an apparent equilibrium between immigration and selection, wMel rose to fixation by 2018. Using analytic approximations and statistical analyses, we demonstrate that the observed fixation of wMel at PE is consistent with both stochastic transition past an unstable threshold frequency and deterministic transformation produced by steady immigration at a rate just above the threshold required for deterministic invasion. The indeterminacy results from a delicate balance of parameters needed to produce the delayed transition observed. Our analyses suggest that once Wolbachia transinfections are established locally through systematic introductions, stochastic “threshold crossing” is likely to only minimally enhance spatial spread, providing a local ratchet that slightly – but systematically – aids area-wide transformation of disease-vector populations in heterogeneous landscapes. AU - Turelli, Michael AU - Barton, Nicholas H ID - 11686 KW - Biological sciences TI - Wolbachia frequency data from: Why did the Wolbachia transinfection cross the road? Drift, deterministic dynamics and disease control ER - TY - JOUR AB - Predicting function from sequence is a central problem of biology. Currently, this is possible only locally in a narrow mutational neighborhood around a wildtype sequence rather than globally from any sequence. Using random mutant libraries, we developed a biophysical model that accounts for multiple features of σ70 binding bacterial promoters to predict constitutive gene expression levels from any sequence. We experimentally and theoretically estimated that 10–20% of random sequences lead to expression and ~80% of non-expressing sequences are one mutation away from a functional promoter. The potential for generating expression from random sequences is so pervasive that selection acts against σ70-RNA polymerase binding sites even within inter-genic, promoter-containing regions. This pervasiveness of σ70-binding sites implies that emergence of promoters is not the limiting step in gene regulatory evolution. Ultimately, the inclusion of novel features of promoter function into a mechanistic model enabled not only more accurate predictions of gene expression levels, but also identified that promoters evolve more rapidly than previously thought. AU - Lagator, Mato AU - Sarikas, Srdjan AU - Steinrueck, Magdalena AU - Toledo-Aparicio, David AU - Bollback, Jonathan P AU - Guet, Calin C AU - Tkačik, Gašper ID - 10736 JF - eLife TI - Predicting bacterial promoter function and evolution from random sequences VL - 11 ER - TY - JOUR AB - Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction. AU - Freitas, Susana AU - Westram, Anja M AU - Schwander, Tanja AU - Arakelyan, Marine AU - Ilgaz, Çetin AU - Kumlutas, Yusuf AU - Harris, David James AU - Carretero, Miguel A. AU - Butlin, Roger K. ID - 11334 IS - 5 JF - Evolution SN - 0014-3820 TI - Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization VL - 76 ER - TY - JOUR AB - Empirical essays of fitness landscapes suggest that they may be rugged, that is having multiple fitness peaks. Such fitness landscapes, those that have multiple peaks, necessarily have special local structures, called reciprocal sign epistasis (Poelwijk et al. in J Theor Biol 272:141–144, 2011). Here, we investigate the quantitative relationship between the number of fitness peaks and the number of reciprocal sign epistatic interactions. Previously, it has been shown (Poelwijk et al. in J Theor Biol 272:141–144, 2011) that pairwise reciprocal sign epistasis is a necessary but not sufficient condition for the existence of multiple peaks. Applying discrete Morse theory, which to our knowledge has never been used in this context, we extend this result by giving the minimal number of reciprocal sign epistatic interactions required to create a given number of peaks. AU - Saona Urmeneta, Raimundo J AU - Kondrashov, Fyodor AU - Khudiakova, Kseniia ID - 11447 IS - 8 JF - Bulletin of Mathematical Biology KW - Computational Theory and Mathematics KW - General Agricultural and Biological Sciences KW - Pharmacology KW - General Environmental Science KW - General Biochemistry KW - Genetics and Molecular Biology KW - General Mathematics KW - Immunology KW - General Neuroscience SN - 0092-8240 TI - Relation between the number of peaks and the number of reciprocal sign epistatic interactions VL - 84 ER - TY - JOUR AB - Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local adaptation and parallel evolution is a major goal of evolutionary genomics. It is now known that by preventing the break-up of favourable combinations of alleles across multiple loci, genetic architectures that reduce recombination, like chromosomal inversions, can make an important contribution to local adaptation. However, little is known about whether inversions also contribute disproportionately to parallel evolution. Our aim here is to highlight this knowledge gap, to showcase existing studies, and to illustrate the differences between genomic architectures with and without inversions using simple models. We predict that by generating stronger effective selection, inversions can sometimes speed up the parallel adaptive process or enable parallel adaptation where it would be impossible otherwise, but this is highly dependent on the spatial setting. We highlight that further empirical work is needed, in particular to cover a broader taxonomic range and to understand the relative importance of inversions compared to genomic regions without inversions. AU - Westram, Anja M AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger AU - Barton, Nicholas H ID - 11546 IS - 1856 JF - Philosophical Transactions of the Royal Society B: Biological Sciences KW - General Agricultural and Biological Sciences KW - General Biochemistry KW - Genetics and Molecular Biology SN - 0962-8436 TI - Inversions and parallel evolution VL - 377 ER - TY - JOUR AB - Spatially explicit population genetic models have long been developed, yet have rarely been used to test hypotheses about the spatial distribution of genetic diversity or the genetic divergence between populations. Here, we use spatially explicit coalescence simulations to explore the properties of the island and the two-dimensional stepping stone models under a wide range of scenarios with spatio-temporal variation in deme size. We avoid the simulation of genetic data, using the fact that under the studied models, summary statistics of genetic diversity and divergence can be approximated from coalescence times. We perform the simulations using gridCoal, a flexible spatial wrapper for the software msprime (Kelleher et al., 2016, Theoretical Population Biology, 95, 13) developed herein. In gridCoal, deme sizes can change arbitrarily across space and time, as well as migration rates between individual demes. We identify different factors that can cause a deviation from theoretical expectations, such as the simulation time in comparison to the effective deme size and the spatio-temporal autocorrelation across the grid. Our results highlight that FST, a measure of the strength of population structure, principally depends on recent demography, which makes it robust to temporal variation in deme size. In contrast, the amount of genetic diversity is dependent on the distant past when Ne is large, therefore longer run times are needed to estimate Ne than FST. Finally, we illustrate the use of gridCoal on a real-world example, the range expansion of silver fir (Abies alba Mill.) since the last glacial maximum, using different degrees of spatio-temporal variation in deme size. AU - Szep, Eniko AU - Trubenova, Barbora AU - Csilléry, Katalin ID - 11640 IS - 8 JF - Molecular Ecology Resources SN - 1755-098X TI - Using gridCoal to assess whether standard population genetic theory holds in the presence of spatio-temporal heterogeneity in population size VL - 22 ER - TY - JOUR AB - Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex-determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex-determining region. Chromosomal inversions may contribute to recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex-determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment-dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well-studied example of local adaptation within a species: the intertidal snail, Littorina saxatilis. Using SNP data from a Swedish hybrid zone, we find novel evidence for a female-heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion-sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex-determining region between ecotypes. Such sex chromosome-environment interactions have not previously been uncovered in L. saxatilis and are known in few other organisms. A combination of both sex-specific selection and divergent natural selection is required to explain these highly unusual patterns. AU - Hearn, Katherine E. AU - Koch, Eva L. AU - Stankowski, Sean AU - Butlin, Roger K. AU - Faria, Rui AU - Johannesson, Kerstin AU - Westram, Anja M ID - 12001 IS - 5 JF - Evolution Letters TI - Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis VL - 6 ER - TY - JOUR AB - Polygenic adaptation is thought to be ubiquitous, yet remains poorly understood. Here, we model this process analytically, in the plausible setting of a highly polygenic, quantitative trait that experiences a sudden shift in the fitness optimum. We show how the mean phenotype changes over time, depending on the effect sizes of loci that contribute to variance in the trait, and characterize the allele dynamics at these loci. Notably, we describe the two phases of the allele dynamics: The first is a rapid phase, in which directional selection introduces small frequency differences between alleles whose effects are aligned with or opposed to the shift, ultimately leading to small differences in their probability of fixation during a second, longer phase, governed by stabilizing selection. As we discuss, key results should hold in more general settings and have important implications for efforts to identify the genetic basis of adaptation in humans and other species. AU - Hayward, Laura AU - Sella, Guy ID - 12157 JF - eLife KW - General Immunology and Microbiology KW - General Biochemistry KW - Genetics and Molecular Biology KW - General Medicine KW - General Neuroscience TI - Polygenic adaptation after a sudden change in environment VL - 11 ER - TY - JOUR AB - Kerstin Johannesson is a marine ecologist and evolutionary biologist based at the Tjärnö Marine Laboratory of the University of Gothenburg, which is situated in the beautiful Kosterhavet National Park on the Swedish west coast. Her work, using marine periwinkles (especially Littorina saxatilis and L. fabalis) as main model systems, has made a remarkable contribution to marine evolutionary biology and our understanding of local adaptation and its genetic underpinnings. AU - Westram, Anja M AU - Butlin, Roger ID - 12166 IS - 1 JF - Molecular Ecology KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0962-1083 TI - Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize VL - 32 ER - TY - JOUR AB - Hybrid speciation—the origin of new species resulting from the hybridization of genetically divergent lineages—was once considered rare, but genomic data suggest that it may occur more often than once thought. In this study, Noguerales and Ortego found genomic evidence supporting the hybrid origin of a grasshopper that is able to exploit a broader range of host plants than either of its putative parents. AU - Stankowski, Sean ID - 12234 IS - 11 JF - Evolution KW - General Agricultural and Biological Sciences KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0014-3820 TI - Digest: On the origin of a possible hybrid species VL - 76 ER - TY - JOUR AB - Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence. AU - Koch, Eva L. AU - Ravinet, Mark AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 12247 IS - 10 JF - Evolution KW - General Agricultural and Biological Sciences KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0014-3820 TI - Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution VL - 76 ER - TY - GEN AB - Chromosomal inversions have been shown to play a major role in local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence. AU - Koch, Eva AU - Ravinet, Mark AU - Westram, Anja M AU - Jonannesson, Kerstin AU - Butlin, Roger ID - 13066 TI - Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution ER - TY - JOUR AB - Reproductive isolation (RI) is a core concept in evolutionary biology. It has been the central focus of speciation research since the modern synthesis and is the basis by which biological species are defined. Despite this, the term is used in seemingly different ways, and attempts to quantify RI have used very different approaches. After showing that the field lacks a clear definition of the term, we attempt to clarify key issues, including what RI is, how it can be quantified in principle, and how it can be measured in practice. Following other definitions with a genetic focus, we propose that RI is a quantitative measure of the effect that genetic differences between populations have on gene flow. Specifically, RI compares the flow of neutral alleles in the presence of these genetic differences to the flow without any such differences. RI is thus greater than zero when genetic differences between populations reduce the flow of neutral alleles between populations. We show how RI can be quantified in a range of scenarios. A key conclusion is that RI depends strongly on circumstances—including the spatial, temporal and genomic context—making it difficult to compare across systems. After reviewing methods for estimating RI from data, we conclude that it is difficult to measure in practice. We discuss our findings in light of the goals of speciation research and encourage the use of methods for estimating RI that integrate organismal and genetic approaches. AU - Westram, Anja M AU - Stankowski, Sean AU - Surendranadh, Parvathy AU - Barton, Nicholas H ID - 12264 IS - 9 JF - Journal of Evolutionary Biology KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 1010-061X TI - What is reproductive isolation? VL - 35 ER - TY - JOUR AU - Westram, Anja M AU - Stankowski, Sean AU - Surendranadh, Parvathy AU - Barton, Nicholas H ID - 12265 IS - 9 JF - Journal of Evolutionary Biology KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 1010-061X TI - Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?’ VL - 35 ER - TY - JOUR AB - A species distributed across diverse environments may adapt to local conditions. We ask how quickly such a species changes its range in response to changed conditions. Szép et al. (Szép E, Sachdeva H, Barton NH. 2021 Polygenic local adaptation in metapopulations: a stochastic eco-evolutionary model. Evolution75, 1030–1045 (doi:10.1111/evo.14210)) used the infinite island model to find the stationary distribution of allele frequencies and deme sizes. We extend this to find how a metapopulation responds to changes in carrying capacity, selection strength, or migration rate when deme sizes are fixed. We further develop a ‘fixed-state’ approximation. Under this approximation, polymorphism is only possible for a narrow range of habitat proportions when selection is weak compared to drift, but for a much wider range otherwise. When rates of selection or migration relative to drift change in a single deme of the metapopulation, the population takes a time of order m−1 to reach the new equilibrium. However, even with many loci, there can be substantial fluctuations in net adaptation, because at each locus, alleles randomly get lost or fixed. Thus, in a finite metapopulation, variation may gradually be lost by chance, even if it would persist in an infinite metapopulation. When conditions change across the whole metapopulation, there can be rapid change, which is predicted well by the fixed-state approximation. This work helps towards an understanding of how metapopulations extend their range across diverse environments. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’. AU - Barton, Nicholas H AU - Olusanya, Oluwafunmilola O ID - 10787 IS - 1848 JF - Philosophical Transactions of the Royal Society B: Biological Sciences KW - General Agricultural and Biological Sciences KW - General Biochemistry KW - Genetics and Molecular Biology SN - 0962-8436 TI - The response of a metapopulation to a changing environment VL - 377 ER - TY - JOUR AB - We analyse how migration from a large mainland influences genetic load and population numbers on an island, in a scenario where fitness-affecting variants are unconditionally deleterious, and where numbers decline with increasing load. Our analysis shows that migration can have qualitatively different effects, depending on the total mutation target and fitness effects of deleterious variants. In particular, we find that populations exhibit a genetic Allee effect across a wide range of parameter combinations, when variants are partially recessive, cycling between low-load (large-population) and high-load (sink) states. Increased migration reduces load in the sink state (by increasing heterozygosity) but further inflates load in the large-population state (by hindering purging). We identify various critical parameter thresholds at which one or other stable state collapses, and discuss how these thresholds are influenced by the genetic versus demographic effects of migration. Our analysis is based on a ‘semi-deterministic’ analysis, which accounts for genetic drift but neglects demographic stochasticity. We also compare against simulations which account for both demographic stochasticity and drift. Our results clarify the importance of gene flow as a key determinant of extinction risk in peripheral populations, even in the absence of ecological gradients. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (part I)’. AU - Sachdeva, Himani AU - Olusanya, Oluwafunmilola O AU - Barton, Nicholas H ID - 10658 IS - 1846 JF - Philosophical Transactions of the Royal Society B SN - 0962-8436 TI - Genetic load and extinction in peripheral populations: The roles of migration, drift and demographic stochasticity VL - 377 ER - TY - JOUR AB - Many studies have quantified the distribution of heterozygosity and relatedness in natural populations, but few have examined the demographic processes driving these patterns. In this study, we take a novel approach by studying how population structure affects both pairwise identity and the distribution of heterozygosity in a natural population of the self-incompatible plant Antirrhinum majus. Excess variance in heterozygosity between individuals is due to identity disequilibrium, which reflects the variance in inbreeding between individuals; it is measured by the statistic g2. We calculated g2 together with FST and pairwise relatedness (Fij) using 91 SNPs in 22,353 individuals collected over 11 years. We find that pairwise Fij declines rapidly over short spatial scales, and the excess variance in heterozygosity between individuals reflects significant variation in inbreeding. Additionally, we detect an excess of individuals with around half the average heterozygosity, indicating either selfing or matings between close relatives. We use 2 types of simulation to ask whether variation in heterozygosity is consistent with fine-scale spatial population structure. First, by simulating offspring using parents drawn from a range of spatial scales, we show that the known pollen dispersal kernel explains g2. Second, we simulate a 1,000-generation pedigree using the known dispersal and spatial distribution and find that the resulting g2 is consistent with that observed from the field data. In contrast, a simulated population with uniform density underestimates g2, indicating that heterogeneous density promotes identity disequilibrium. Our study shows that heterogeneous density and leptokurtic dispersal can together explain the distribution of heterozygosity. AU - Surendranadh, Parvathy AU - Arathoon, Louise S AU - Baskett, Carina AU - Field, David AU - Pickup, Melinda AU - Barton, Nicholas H ID - 11411 IS - 3 JF - Genetics TI - Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus VL - 221 ER - TY - DATA AB - Here are the research data underlying the publication "Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus" Further information are summed up in the README document. AU - Surendranadh, Parvathy AU - Arathoon, Louise S AU - Baskett, Carina AU - Field, David AU - Pickup, Melinda AU - Barton, Nicholas H ID - 11321 TI - Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus ER - TY - JOUR AB - Selection accumulates information in the genome—it guides stochastically evolving populations toward states (genotype frequencies) that would be unlikely under neutrality. This can be quantified as the Kullback–Leibler (KL) divergence between the actual distribution of genotype frequencies and the corresponding neutral distribution. First, we show that this population-level information sets an upper bound on the information at the level of genotype and phenotype, limiting how precisely they can be specified by selection. Next, we study how the accumulation and maintenance of information is limited by the cost of selection, measured as the genetic load or the relative fitness variance, both of which we connect to the control-theoretic KL cost of control. The information accumulation rate is upper bounded by the population size times the cost of selection. This bound is very general, and applies across models (Wright–Fisher, Moran, diffusion) and to arbitrary forms of selection, mutation, and recombination. Finally, the cost of maintaining information depends on how it is encoded: Specifying a single allele out of two is expensive, but one bit encoded among many weakly specified loci (as in a polygenic trait) is cheap. AU - Hledik, Michal AU - Barton, Nicholas H AU - Tkačik, Gašper ID - 12081 IS - 36 JF - Proceedings of the National Academy of Sciences SN - 0027-8424 TI - Accumulation and maintenance of information in evolution VL - 119 ER - TY - THES AB - In evolve and resequence experiments, a population is sequenced, subjected to selection and then sequenced again, so that genetic changes before and after selection can be observed at the genetic level. Here, I use these studies to better understand the genetic basis of complex traits - traits which depend on more than a few genes. In the first chapter, I discuss the first evolve and resequence experiment, in which a population of mice, the so-called "Longshanks" mice, were selected for tibia length while their body mass was kept constant. The full pedigree is known. We observed a selection response on all chromosomes and used the infinitesimal model with linkage, a model which assumes an infinite number of genes with infinitesimally small effect sizes, as a null model. Results implied a very polygenic basis with a few loci of major effect standing out and changing in parallel. There was large variability between the different chromosomes in this study, probably due to LD. In chapter two, I go on to discuss the impact of LD, on the variability in an allele-frequency based summary statistic, giving an equation based on the initial allele frequencies, average pairwise LD, and the first four moments of the haplotype block copy number distribution. I describe this distribution by referring back to the founder generation. I then demonstrate how to infer selection via a maximum likelihood scheme on the example of a single locus and discuss how to extend this to more realistic scenarios. In chapter three, I discuss the second evolve and resequence experiment, in which a small population of Drosophila melanogaster was selected for increased pupal case size over 6 generations. The experiment was highly replicated with 27 lines selected within family and a known pedigree. We observed a phenotypic selection response of over one standard deviation. I describe the patterns in allele frequency data, including allele frequency changes and patterns of heterozygosity, and give ideas for future work. AU - Belohlavy, Stefanie ID - 11388 SN - 978-3-99078-018-3 TI - The genetic basis of complex traits studied via analysis of evolve and resequence experiments ER - TY - JOUR AB - Realistic models of biological processes typically involve interacting components on multiple scales, driven by changing environment and inherent stochasticity. Such models are often analytically and numerically intractable. We revisit a dynamic maximum entropy method that combines a static maximum entropy with a quasi-stationary approximation. This allows us to reduce stochastic non-equilibrium dynamics expressed by the Fokker-Planck equation to a simpler low-dimensional deterministic dynamics, without the need to track microscopic details. Although the method has been previously applied to a few (rather complicated) applications in population genetics, our main goal here is to explain and to better understand how the method works. We demonstrate the usefulness of the method for two widely studied stochastic problems, highlighting its accuracy in capturing important macroscopic quantities even in rapidly changing non-stationary conditions. For the Ornstein-Uhlenbeck process, the method recovers the exact dynamics whilst for a stochastic island model with migration from other habitats, the approximation retains high macroscopic accuracy under a wide range of scenarios in a dynamic environment. AU - Bod'ová, Katarína AU - Szep, Eniko AU - Barton, Nicholas H ID - 10535 IS - 12 JF - PLoS Computational Biology SN - 1553-734X TI - Dynamic maximum entropy provides accurate approximation of structured population dynamics VL - 17 ER - TY - JOUR AB - The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study ‘replicated’ instances of secondary contact between closely related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry‐informative panel of such SNPs. We then compared their frequencies in newly sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi‐stable variants (Dobzhansky‐Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact. AU - Simon, Alexis AU - Fraisse, Christelle AU - El Ayari, Tahani AU - Liautard‐Haag, Cathy AU - Strelkov, Petr AU - Welch, John J AU - Bierne, Nicolas ID - 8708 IS - 1 JF - Journal of Evolutionary Biology SN - 1010061X TI - How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels VL - 34 ER - TY - JOUR AB - Montane cloud forests are areas of high endemism, and are one of the more vulnerable terrestrial ecosystems to climate change. Thus, understanding how they both contribute to the generation of biodiversity, and will respond to ongoing climate change, are important and related challenges. The widely accepted model for montane cloud forest dynamics involves upslope forcing of their range limits with global climate warming. However, limited climate data provides some support for an alternative model, where range limits are forced downslope with climate warming. Testing between these two models is challenging, due to the inherent limitations of climate and pollen records. We overcome this with an alternative source of historical information, testing between competing model predictions using genomic data and demographic analyses for a species of beetle tightly associated to an oceanic island cloud forest. Results unequivocally support the alternative model: populations that were isolated at higher elevation peaks during the Last Glacial Maximum are now in contact and hybridizing at lower elevations. Our results suggest that genomic data are a rich source of information to further understand how montane cloud forest biodiversity originates, and how it is likely to be impacted by ongoing climate change. AU - Salces-Castellano, Antonia AU - Stankowski, Sean AU - Arribas, Paula AU - Patino, Jairo AU - Karger, Dirk N. AU - Butlin, Roger AU - Emerson, Brent C. ID - 8743 IS - 2 JF - Evolution SN - 0014-3820 TI - Long-term cloud forest response to climate warming revealed by insect speciation history VL - 75 ER - TY - JOUR AB - Domestication is a human‐induced selection process that imprints the genomes of domesticated populations over a short evolutionary time scale and that occurs in a given demographic context. Reconstructing historical gene flow, effective population size changes and their timing is therefore of fundamental interest to understand how plant demography and human selection jointly shape genomic divergence during domestication. Yet, the comparison under a single statistical framework of independent domestication histories across different crop species has been little evaluated so far. Thus, it is unclear whether domestication leads to convergent demographic changes that similarly affect crop genomes. To address this question, we used existing and new transcriptome data on three crop species of Solanaceae (eggplant, pepper and tomato), together with their close wild relatives. We fitted twelve demographic models of increasing complexity on the unfolded joint allele frequency spectrum for each wild/crop pair, and we found evidence for both shared and species‐specific demographic processes between species. A convergent history of domestication with gene flow was inferred for all three species, along with evidence of strong reduction in the effective population size during the cultivation stage of tomato and pepper. The absence of any reduction in size of the crop in eggplant stands out from the classical view of the domestication process; as does the existence of a “protracted period” of management before cultivation. Our results also suggest divergent management strategies of modern cultivars among species as their current demography substantially differs. Finally, the timing of domestication is species‐specific and supported by the few historical records available. AU - Arnoux, Stéphanie AU - Fraisse, Christelle AU - Sauvage, Christopher ID - 8928 IS - 2 JF - Journal of Evolutionary Biology SN - 1010061X TI - Genomic inference of complex domestication histories in three Solanaceae species VL - 34 ER - TY - JOUR AB - Marine environments are inhabited by a broad representation of the tree of life, yet our understanding of speciation in marine ecosystems is extremely limited compared with terrestrial and freshwater environments. Developing a more comprehensive picture of speciation in marine environments requires that we 'dive under the surface' by studying a wider range of taxa and ecosystems is necessary for a more comprehensive picture of speciation. Although studying marine evolutionary processes is often challenging, recent technological advances in different fields, from maritime engineering to genomics, are making it increasingly possible to study speciation of marine life forms across diverse ecosystems and taxa. Motivated by recent research in the field, including the 14 contributions in this issue, we highlight and discuss six axes of research that we think will deepen our understanding of speciation in the marine realm: (a) study a broader range of marine environments and organisms; (b) identify the reproductive barriers driving speciation between marine taxa; (c) understand the role of different genomic architectures underlying reproductive isolation; (d) infer the evolutionary history of divergence using model‐based approaches; (e) study patterns of hybridization and introgression between marine taxa; and (f) implement highly interdisciplinary, collaborative research programmes. In outlining these goals, we hope to inspire researchers to continue filling this critical knowledge gap surrounding the origins of marine biodiversity. AU - Faria, Rui AU - Johannesson, Kerstin AU - Stankowski, Sean ID - 9100 IS - 1 JF - Journal of Evolutionary Biology SN - 1010061X TI - Speciation in marine environments: Diving under the surface VL - 34 ER - TY - JOUR AB - Interspecific crossing experiments have shown that sex chromosomes play a major role in reproductive isolation between many pairs of species. However, their ability to act as reproductive barriers, which hamper interspecific genetic exchange, has rarely been evaluated quantitatively compared to Autosomes. This genome-wide limitation of gene flow is essential for understanding the complete separation of species, and thus speciation. Here, we develop a mainland-island model of secondary contact between hybridizing species of an XY (or ZW) sexual system. We obtain theoretical predictions for the frequency of introgressed alleles, and the strength of the barrier to neutral gene flow for the two types of chromosomes carrying multiple interspecific barrier loci. Theoretical predictions are obtained for scenarios where introgressed alleles are rare. We show that the same analytical expressions apply for sex chromosomes and autosomes, but with different sex-averaged effective parameters. The specific features of sex chromosomes (hemizygosity and absence of recombination in the heterogametic sex) lead to reduced levels of introgression on the X (or Z) compared to autosomes. This effect can be enhanced by certain types of sex-biased forces, but it remains overall small (except when alleles causing incompatibilities are recessive). We discuss these predictions in the light of empirical data comprising model-based tests of introgression and cline surveys in various biological systems. AU - Fraisse, Christelle AU - Sachdeva, Himani ID - 9168 IS - 2 JF - Genetics SN - 1943-2631 TI - The rates of introgression and barriers to genetic exchange between hybridizing species: Sex chromosomes vs autosomes VL - 217 ER - TY - JOUR AB - We present DILS, a deployable statistical analysis platform for conducting demographic inferences with linked selection from population genomic data using an Approximate Bayesian Computation framework. DILS takes as input single‐population or two‐population data sets (multilocus fasta sequences) and performs three types of analyses in a hierarchical manner, identifying: (a) the best demographic model to study the importance of gene flow and population size change on the genetic patterns of polymorphism and divergence, (b) the best genomic model to determine whether the effective size Ne and migration rate N, m are heterogeneously distributed along the genome (implying linked selection) and (c) loci in genomic regions most associated with barriers to gene flow. Also available via a Web interface, an objective of DILS is to facilitate collaborative research in speciation genomics. Here, we show the performance and limitations of DILS by using simulations and finally apply the method to published data on a divergence continuum composed by 28 pairs of Mytilus mussel populations/species. AU - Fraisse, Christelle AU - Popovic, Iva AU - Mazoyer, Clément AU - Spataro, Bruno AU - Delmotte, Stéphane AU - Romiguier, Jonathan AU - Loire, Étienne AU - Simon, Alexis AU - Galtier, Nicolas AU - Duret, Laurent AU - Bierne, Nicolas AU - Vekemans, Xavier AU - Roux, Camille ID - 9119 JF - Molecular Ecology Resources SN - 1755098X TI - DILS: Demographic inferences with linked selection by using ABC VL - 21 ER - TY - JOUR AB - Genetic variation segregates as linked sets of variants, or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. And yet, genomic data often lack haplotype information, due to constraints in sequencing technologies. Here we present “haplotagging”, a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabase-size haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high- and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species the geographic clines for the major wing pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the centre of the hybrid zone. We propose that shared warning signalling (Müllerian mimicry) may couple the cline shifts seen in both species, and facilitate the parallel co-emergence of a novel hybrid morph in both co-mimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations. AU - Meier, Joana I. AU - Salazar, Patricio A. AU - Kučka, Marek AU - Davies, Robert William AU - Dréau, Andreea AU - Aldás, Ismael AU - Power, Olivia Box AU - Nadeau, Nicola J. AU - Bridle, Jon R. AU - Rolian, Campbell AU - Barton, Nicholas H AU - McMillan, W. Owen AU - Jiggins, Chris D. AU - Chan, Yingguang Frank ID - 9375 IS - 25 JF - PNAS TI - Haplotype tagging reveals parallel formation of hybrid races in two butterfly species VL - 118 ER - TY - JOUR AB - Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on phenotypes under divergent selection. For this, the marine snail Littorina saxatilis provides an ideal study system. Divergent ecotypes adapted to wave action and crab predation occur in close proximity on intertidal shores with gene flow between them. Here, we used F2 individuals obtained from crosses between the ecotypes to test for associations between genomic regions and traits distinguishing the Crab‐/Wave‐adapted ecotypes including size, shape, shell thickness, and behavior. We show that most of these traits are influenced by two previously detected inversion regions that are divergent between ecotypes. We thus gain a better understanding of one important underlying mechanism responsible for the rapid and repeated formation of ecotypes: divergent selection acting on inversions. We also found that some inversions contributed to more than one trait suggesting that they may contain several loci involved in adaptation, consistent with the hypothesis that suppression of recombination within inversions facilitates differentiation in the presence of gene flow. AU - Koch, Eva L. AU - Morales, Hernán E. AU - Larsson, Jenny AU - Westram, Anja M AU - Faria, Rui AU - Lemmon, Alan R. AU - Lemmon, E. Moriarty AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 9394 IS - 3 JF - Evolution Letters TI - Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis VL - 5 ER - TY - JOUR AB - Humans conceptualize the diversity of life by classifying individuals into types we call ‘species’1. The species we recognize influence political and financial decisions and guide our understanding of how units of diversity evolve and interact. Although the idea of species may seem intuitive, a debate about the best way to define them has raged even before Darwin2. So much energy has been devoted to the so-called ‘species problem’ that no amount of discourse will ever likely solve it2,3. Dozens of species concepts are currently recognized3, but we lack a concrete understanding of how much researchers actually disagree and the factors that cause them to think differently1,2. To address this, we used a survey to quantify the species problem for the first time. The results indicate that the disagreement is extensive: two randomly chosen respondents will most likely disagree on the nature of species. The probability of disagreement is not predicted by researcher experience or broad study system, but tended to be lower among researchers with similar focus, training and who study the same organism. Should we see this diversity of perspectives as a problem? We argue that we should not. AU - Stankowski, Sean AU - Ravinet, Mark ID - 9392 IS - 9 JF - Current Biology SN - 09609822 TI - Quantifying the use of species concepts VL - 31 ER - TY - GEN AB - Chromosomal inversion polymorphisms, segments of chromosomes that are flipped in orientation and occur in reversed order in some individuals, have long been recognized to play an important role in local adaptation. They can reduce recombination in heterozygous individuals and thus help to maintain sets of locally adapted alleles. In a wide range of organisms, populations adapted to different habitats differ in frequency of inversion arrangements. However, getting a full understanding of the importance of inversions for adaptation requires confirmation of their influence on traits under divergent selection. Here, we studied a marine snail, Littorina saxatilis, that has evolved ecotypes adapted to wave exposure or crab predation. These two types occur in close proximity on different parts of the shore. Gene flow between them exists in contact zones. However, they exhibit strong phenotypic divergence in several traits under habitat-specific selection, including size, shape and behaviour. We used crosses between these ecotypes to identify genomic regions that explain variation in these traits by using QTL analysis and variance partitioning across linkage groups. We could show that previously detected inversion regions contribute to adaptive divergence. Some inversions influenced multiple traits suggesting that they contain sets of locally adaptive alleles. Our study also identified regions without known inversions that are important for phenotypic divergence. Thus, we provide a more complete overview of the importance of inversions in relation to the remaining genome. AU - Koch, Eva AU - Morales, Hernán E. AU - Larsson, Jenny AU - Westram, Anja M AU - Faria, Rui AU - Lemmon, Alan R. AU - Lemmon, E. Moriarty AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 12987 TI - Data from: Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis ER - TY - JOUR AB - Antibiotic concentrations vary dramatically in the body and the environment. Hence, understanding the dynamics of resistance evolution along antibiotic concentration gradients is critical for predicting and slowing the emergence and spread of resistance. While it has been shown that increasing the concentration of an antibiotic slows resistance evolution, how adaptation to one antibiotic concentration correlates with fitness at other points along the gradient has not received much attention. Here, we selected populations of Escherichia coli at several points along a concentration gradient for three different antibiotics, asking how rapidly resistance evolved and whether populations became specialized to the antibiotic concentration they were selected on. Populations selected at higher concentrations evolved resistance more slowly but exhibited equal or higher fitness across the whole gradient. Populations selected at lower concentrations evolved resistance rapidly, but overall fitness in the presence of antibiotics was lower. However, these populations readily adapted to higher concentrations upon subsequent selection. Our results indicate that resistance management strategies must account not only for the rates of resistance evolution but also for the fitness of evolved strains. AU - Lagator, Mato AU - Uecker, Hildegard AU - Neve, Paul ID - 9410 IS - 5 JF - Biology letters TI - Adaptation at different points along antibiotic concentration gradients VL - 17 ER - TY - JOUR AB - A key step in understanding the genetic basis of different evolutionary outcomes (e.g., adaptation) is to determine the roles played by different mutation types (e.g., SNPs, translocations and inversions). To do this we must simultaneously consider different mutation types in an evolutionary framework. Here, we propose a research framework that directly utilizes the most important characteristics of mutations, their population genetic effects, to determine their relative evolutionary significance in a given scenario. We review known population genetic effects of different mutation types and show how these may be connected to different evolutionary outcomes. We provide examples of how to implement this framework and pinpoint areas where more data, theory and synthesis are needed. Linking experimental and theoretical approaches to examine different mutation types simultaneously is a critical step towards understanding their evolutionary significance. AU - Berdan, Emma L. AU - Blanckaert, Alexandre AU - Slotte, Tanja AU - Suh, Alexander AU - Westram, Anja M AU - Fragata, Inês ID - 9470 IS - 12 JF - Molecular Ecology SN - 09621083 TI - Unboxing mutations: Connecting mutation types with evolutionary consequences VL - 30 ER - TY - JOUR AB - Aims: Mass antigen testing programs have been challenged because of an alleged insufficient specificity, leading to a large number of false positives. The objective of this study is to derive a lower bound of the specificity of the SD Biosensor Standard Q Ag-Test in large scale practical use. Methods: Based on county data from the nationwide tests for SARS-CoV-2 in Slovakia between 31.10.–1.11. 2020 we calculate a lower confidence bound for the specificity. As positive test results were not systematically verified by PCR tests, we base the lower bound on a worst case assumption, assuming all positives to be false positives. Results: 3,625,332 persons from 79 counties were tested. The lowest positivity rate was observed in the county of Rožňava where 100 out of 34307 (0.29%) tests were positive. This implies a test specificity of at least 99.6% (97.5% one-sided lower confidence bound, adjusted for multiplicity). Conclusion: The obtained lower bound suggests a higher specificity compared to earlier studies in spite of the underlying worst case assumption and the application in a mass testing setting. The actual specificity is expected to exceed 99.6% if the prevalence in the respective regions was non-negligible at the time of testing. To our knowledge, this estimate constitutes the first bound obtained from large scale practical use of an antigen test. AU - Hledik, Michal AU - Polechova, Jitka AU - Beiglböck, Mathias AU - Herdina, Anna Nele AU - Strassl, Robert AU - Posch, Martin ID - 9816 IS - 7 JF - PLoS ONE TI - Analysis of the specificity of a COVID-19 antigen test in the Slovak mass testing program VL - 16 ER - TY - JOUR AB - This paper analyses the conditions for local adaptation in a metapopulation with infinitely many islands under a model of hard selection, where population size depends on local fitness. Each island belongs to one of two distinct ecological niches or habitats. Fitness is influenced by an additive trait which is under habitat‐dependent directional selection. Our analysis is based on the diffusion approximation and accounts for both genetic drift and demographic stochasticity. By neglecting linkage disequilibria, it yields the joint distribution of allele frequencies and population size on each island. We find that under hard selection, the conditions for local adaptation in a rare habitat are more restrictive for more polygenic traits: even moderate migration load per locus at very many loci is sufficient for population sizes to decline. This further reduces the efficacy of selection at individual loci due to increased drift and because smaller populations are more prone to swamping due to migration, causing a positive feedback between increasing maladaptation and declining population sizes. Our analysis also highlights the importance of demographic stochasticity, which exacerbates the decline in numbers of maladapted populations, leading to population collapse in the rare habitat at significantly lower migration than predicted by deterministic arguments. AU - Szep, Eniko AU - Sachdeva, Himani AU - Barton, Nicholas H ID - 9252 IS - 5 JF - Evolution KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics KW - General Agricultural and Biological Sciences SN - 0014-3820 TI - Polygenic local adaptation in metapopulations: A stochastic eco‐evolutionary model VL - 75 ER - TY - JOUR AB - If there are no constraints on the process of speciation, then the number of species might be expected to match the number of available niches and this number might be indefinitely large. One possible constraint is the opportunity for allopatric divergence. In 1981, Felsenstein used a simple and elegant model to ask if there might also be genetic constraints. He showed that progress towards speciation could be described by the build‐up of linkage disequilibrium among divergently selected loci and between these loci and those contributing to other forms of reproductive isolation. Therefore, speciation is opposed by recombination, because it tends to break down linkage disequilibria. Felsenstein then introduced a crucial distinction between “two‐allele” models, which are subject to this effect, and “one‐allele” models, which are free from the recombination constraint. These fundamentally important insights have been the foundation for both empirical and theoretical studies of speciation ever since. AU - Butlin, Roger K. AU - Servedio, Maria R. AU - Smadja, Carole M. AU - Bank, Claudia AU - Barton, Nicholas H AU - Flaxman, Samuel M. AU - Giraud, Tatiana AU - Hopkins, Robin AU - Larson, Erica L. AU - Maan, Martine E. AU - Meier, Joana AU - Merrill, Richard AU - Noor, Mohamed A. F. AU - Ortiz‐Barrientos, Daniel AU - Qvarnström, Anna ID - 9374 IS - 5 JF - Evolution KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics KW - General Agricultural and Biological Sciences SN - 0014-3820 TI - Homage to Felsenstein 1981, or why are there so few/many species? VL - 75 ER - TY - GEN AB - This paper analyzes the conditions for local adaptation in a metapopulation with infinitely many islands under a model of hard selection, where population size depends on local fitness. Each island belongs to one of two distinct ecological niches or habitats. Fitness is influenced by an additive trait which is under habitat-dependent directional selection. Our analysis is based on the diffusion approximation and accounts for both genetic drift and demographic stochasticity. By neglecting linkage disequilibria, it yields the joint distribution of allele frequencies and population size on each island. We find that under hard selection, the conditions for local adaptation in a rare habitat are more restrictive for more polygenic traits: even moderate migration load per locus at very many loci is sufficient for population sizes to decline. This further reduces the efficacy of selection at individual loci due to increased drift and because smaller populations are more prone to swamping due to migration, causing a positive feedback between increasing maladaptation and declining population sizes. Our analysis also highlights the importance of demographic stochasticity, which exacerbates the decline in numbers of maladapted populations, leading to population collapse in the rare habitat at significantly lower migration than predicted by deterministic arguments. AU - Szep, Eniko AU - Sachdeva, Himani AU - Barton, Nicholas H ID - 13062 TI - Supplementary code for: Polygenic local adaptation in metapopulations: A stochastic eco-evolutionary model ER - TY - JOUR AB - A primary roadblock to our understanding of speciation is that it usually occurs over a timeframe that is too long to study from start to finish. The idea of a speciation continuum provides something of a solution to this problem; rather than observing the entire process, we can simply reconstruct it from the multitude of speciation events that surround us. But what do we really mean when we talk about the speciation continuum, and can it really help us understand speciation? We explored these questions using a literature review and online survey of speciation researchers. Although most researchers were familiar with the concept and thought it was useful, our survey revealed extensive disagreement about what the speciation continuum actually tells us. This is due partly to the lack of a clear definition. Here, we provide an explicit definition that is compatible with the Biological Species Concept. That is, the speciation continuum is a continuum of reproductive isolation. After outlining the logic of the definition in light of alternatives, we explain why attempts to reconstruct the speciation process from present‐day populations will ultimately fail. We then outline how we think the speciation continuum concept can continue to act as a foundation for understanding the continuum of reproductive isolation that surrounds us. AU - Stankowski, Sean AU - Ravinet, Mark ID - 9383 IS - 6 JF - Evolution SN - 0014-3820 TI - Defining the speciation continuum VL - 75 ER - TY - CHAP AB - Hybrid zones are narrow geographic regions where different populations, races or interbreeding species meet and mate, producing mixed ‘hybrid’ offspring. They are relatively common and can be found in a diverse range of organisms and environments. The study of hybrid zones has played an important role in our understanding of the origin of species, with hybrid zones having been described as ‘natural laboratories’. This is because they allow us to study,in situ, the conditions and evolutionary forces that enable divergent taxa to remain distinct despite some ongoing gene exchange between them. AU - Stankowski, Sean AU - Shipilina, Daria AU - Westram, Anja M ID - 14984 SN - 9780470016176 T2 - Encyclopedia of Life Sciences TI - Hybrid Zones VL - 2 ER - TY - DATA AB - Here are the research data underlying the publication " Effects of fine-scale population structure on inbreeding in a long-term study of snapdragons (Antirrhinum majus)." Further information are summed up in the README document. AU - Surendranadh, Parvathy AU - Arathoon, Louise S AU - Baskett, Carina AU - Field, David AU - Pickup, Melinda AU - Barton, Nicholas H ID - 9192 TI - Effects of fine-scale population structure on the distribution of heterozygosity in a long-term study of Antirrhinum majus ER - TY - JOUR AB - The growth of snail shells can be described by simple mathematical rules. Variation in a few parameters can explain much of the diversity of shell shapes seen in nature. However, empirical studies of gastropod shell shape variation typically use geometric morphometric approaches, which do not capture this growth pattern. We have developed a way to infer a set of developmentally descriptive shape parameters based on three-dimensional logarithmic helicospiral growth and using landmarks from two-dimensional shell images as input. We demonstrate the utility of this approach, and compare it to the geometric morphometric approach, using a large set of Littorina saxatilis shells in which locally adapted populations differ in shape. Our method can be modified easily to make it applicable to a wide range of shell forms, which would allow for investigations of the similarities and differences between and within many different species of gastropods. AU - Larsson, J. AU - Westram, Anja M AU - Bengmark, S. AU - Lundh, T. AU - Butlin, R. K. ID - 7651 IS - 163 JF - Journal of The Royal Society Interface SN - 1742-5689 TI - A developmentally descriptive method for quantifying shape in gastropod shells VL - 17 ER - TY - CHAP AB - Inversions are chromosomal rearrangements where the order of genes is reversed. Inversions originate by mutation and can be under positive, negative or balancing selection. Selective effects result from potential disruptive effects on meiosis, gene disruption at inversion breakpoints and, importantly, the effects of inversions as modifiers of recombination rate: Recombination is strongly reduced in individuals heterozygous for an inversion, allowing for alleles at different loci to be inherited as a ‘block’. This may lead to a selective advantage whenever it is favourable to keep certain combinations of alleles associated, for example under local adaptation with gene flow. Inversions can cover a considerable part of a chromosome and contain numerous loci under different selection pressures, so that the resulting overall effects may be complex. Empirical data from various systems show that inversions may have a prominent role in local adaptation, speciation, parallel evolution, the maintenance of polymorphism and sex chromosome evolution. AU - Westram, Anja M AU - Faria, Rui AU - Butlin, Roger AU - Johannesson, Kerstin ID - 9123 SN - 9780470016176 T2 - eLS TI - Inversions and Evolution ER - TY - GEN AB - The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study "replicated" instances of secondary contact between closely-related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry-informative panel of such SNPs. We then compared their frequencies in newly-sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi-stable variants (Dobzhansky-Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact. AU - Simon, Alexis AU - Fraisse, Christelle AU - El Ayari, Tahani AU - Liautard-Haag, Cathy AU - Strelkov, Petr AU - Welch, John AU - Bierne, Nicolas ID - 13073 TI - How do species barriers decay? concordance and local introgression in mosaic hybrid zones of mussels ER - TY - GEN AB - Domestication is a human-induced selection process that imprints the genomes of domesticated populations over a short evolutionary time scale, and that occurs in a given demographic context. Reconstructing historical gene flow, effective population size changes and their timing is therefore of fundamental interest to understand how plant demography and human selection jointly shape genomic divergence during domestication. Yet, the comparison under a single statistical framework of independent domestication histories across different crop species has been little evaluated so far. Thus, it is unclear whether domestication leads to convergent demographic changes that similarly affect crop genomes. To address this question, we used existing and new transcriptome data on three crop species of Solanaceae (eggplant, pepper and tomato), together with their close wild relatives. We fitted twelve demographic models of increasing complexity on the unfolded joint allele frequency spectrum for each wild/crop pair, and we found evidence for both shared and species-specific demographic processes between species. A convergent history of domestication with gene-flow was inferred for all three species, along with evidence of strong reduction in the effective population size during the cultivation stage of tomato and pepper. The absence of any reduction in size of the crop in eggplant stands out from the classical view of the domestication process; as does the existence of a “protracted period” of management before cultivation. Our results also suggest divergent management strategies of modern cultivars among species as their current demography substantially differs. Finally, the timing of domestication is species-specific and supported by the few historical records available. AU - Arnoux, Stephanie AU - Fraisse, Christelle AU - Sauvage, Christopher ID - 13065 TI - VCF files of synonymous SNPs related to: Genomic inference of complex domestication histories in three Solanaceae species ER - TY - JOUR AB - When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple‐effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis , occur in North Atlantic rocky‐shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size‐assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment. AU - Perini, Samuel AU - Rafajlović, Marina AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 7995 IS - 7 JF - Evolution SN - 00143820 TI - Assortative mating, sexual selection, and their consequences for gene flow in Littorina VL - 74 ER - TY - GEN AB - When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple-effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis, occur in North Atlantic rocky-shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size-assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively-sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment. AU - Perini, Samuel AU - Rafajlovic, Marina AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger ID - 8809 TI - Data from: Assortative mating, sexual selection and their consequences for gene flow in Littorina ER - TY - JOUR AU - Barton, Nicholas H ID - 8112 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences SN - 0962-8436 TI - On the completion of speciation VL - 375 ER - TY - JOUR AB - Speciation, that is, the evolution of reproductive barriers eventually leading to complete isolation, is a crucial process generating biodiversity. Recent work has contributed much to our understanding of how reproductive barriers begin to evolve, and how they are maintained in the face of gene flow. However, little is known about the transition from partial to strong reproductive isolation (RI) and the completion of speciation. We argue that the evolution of strong RI is likely to involve different processes, or new interactions among processes, compared with the evolution of the first reproductive barriers. Transition to strong RI may be brought about by changing external conditions, for example, following secondary contact. However, the increasing levels of RI themselves create opportunities for new barriers to evolve and, and interaction or coupling among barriers. These changing processes may depend on genomic architecture and leave detectable signals in the genome. We outline outstanding questions and suggest more theoretical and empirical work, considering both patterns and processes associated with strong RI, is needed to understand how speciation is completed. AU - Kulmuni, Jonna AU - Butlin, Roger K. AU - Lucek, Kay AU - Savolainen, Vincent AU - Westram, Anja M ID - 8168 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological sciences SN - 0962-8436 TI - Towards the completion of speciation: The evolution of reproductive isolation beyond the first barriers VL - 375 ER - TY - JOUR AB - The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions. AU - Stankowski, Sean AU - Westram, Anja M AU - Zagrodzka, Zuzanna B. AU - Eyres, Isobel AU - Broquet, Thomas AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 8167 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences TI - The evolution of strong reproductive isolation between sympatric intertidal snails VL - 375 ER - TY - JOUR AB - Many recent studies have addressed the mechanisms operating during the early stages of speciation, but surprisingly few studies have tested theoretical predictions on the evolution of strong reproductive isolation (RI). To help address this gap, we first undertook a quantitative review of the hybrid zone literature for flowering plants in relation to reproductive barriers. Then, using Populus as an exemplary model group, we analysed genome-wide variation for phylogenetic tree topologies in both early- and late-stage speciation taxa to determine how these patterns may be related to the genomic architecture of RI. Our plant literature survey revealed variation in barrier complexity and an association between barrier number and introgressive gene flow. Focusing on Populus, our genome-wide analysis of tree topologies in speciating poplar taxa points to unusually complex genomic architectures of RI, consistent with earlier genome-wide association studies. These architectures appear to facilitate the ‘escape’ of introgressed genome segments from polygenic barriers even with strong RI, thus affecting their relationships with recombination rates. Placed within the context of the broader literature, our data illustrate how phylogenomic approaches hold great promise for addressing the evolution and temporary breakdown of RI during late stages of speciation. AU - Shang, Huiying AU - Hess, Jaqueline AU - Pickup, Melinda AU - Field, David AU - Ingvarsson, Pär K. AU - Liu, Jianquan AU - Lexer, Christian ID - 8169 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences TI - Evolution of strong reproductive isolation in plants: Broad-scale patterns and lessons from a perennial model group VL - 375 ER - TY - GEN AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA. Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 9799 TI - Simulation code for Fig S1 from the distribution of epistasis on simple fitness landscapes ER - TY - GEN AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA. Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 9798 TI - Simulation code for Fig S2 from the distribution of epistasis on simple fitness landscapes ER - TY - JOUR AB - The biotic interactions hypothesis posits that biotic interactions are more important drivers of adaptation closer to the equator, evidenced by “stronger” contemporary interactions (e.g. greater interaction rates) and/or patterns of trait evolution consistent with a history of stronger interactions. Support for the hypothesis is mixed, but few studies span tropical and temperate regions while experimentally controlling for evolutionary history. Here, we integrate field observations and common garden experiments to quantify the relative importance of pollination and herbivory in a pair of tropical‐temperate congeneric perennial herbs. Phytolacca rivinoides and P. americana are pioneer species native to the Neotropics and the eastern USA, respectively. We compared plant‐pollinator and plant‐herbivore interactions between three tropical populations of P. rivinoides from Costa Rica and three temperate populations of P. americana from its northern range edge in Michigan and Ohio. For some metrics of interaction importance, we also included three subtropical populations of P. americana from its southern range edge in Florida. This approach confounds species and region but allows us, uniquely, to measure complementary proxies of interaction importance across a tropical‐temperate range in one system. To test the prediction that lower‐latitude plants are more reliant on insect pollinators, we quantified floral display and reward, insect visitation rates, and self‐pollination ability (autogamy). To test the prediction that lower‐latitude plants experience more herbivore pressure, we quantified herbivory rates, herbivore abundance, and leaf palatability. We found evidence supporting the biotic interactions hypothesis for most comparisons between P. rivinoides and north‐temperate P. americana (floral display, insect visitation, autogamy, herbivory, herbivore abundance, and young‐leaf palatability). Results for subtropical P. americana populations, however, were typically not intermediate between P. rivinoides and north‐temperate P. americana, as would be predicted by a linear latitudinal gradient in interaction importance. Subtropical young‐leaf palatability was intermediate, but subtropical mature leaves were the least palatable, and pollination‐related traits did not differ between temperate and subtropical regions. These nonlinear patterns of interaction importance suggest future work to relate interaction importance to climatic or biotic thresholds. In sum, we found that the biotic interactions hypothesis was more consistently supported at the larger spatial scale of our study. AU - Baskett, Carina AU - Schroeder, Lucy AU - Weber, Marjorie G. AU - Schemske, Douglas W. ID - 7236 IS - 1 JF - Ecological Monographs SN - 0012-9615 TI - Multiple metrics of latitudinal patterns in insect pollination and herbivory for a tropical‐temperate congener pair VL - 90 ER - TY - JOUR AB - Genetic incompatibilities contribute to reproductive isolation between many diverging populations, but it is still unclear to what extent they play a role if divergence happens with gene flow. In contact zones between the "Crab" and "Wave" ecotypes of the snail Littorina saxatilis, divergent selection forms strong barriers to gene flow, while the role of post‐zygotic barriers due to selection against hybrids remains unclear. High embryo abortion rates in this species could indicate the presence of such barriers. Post‐zygotic barriers might include genetic incompatibilities (e.g. Dobzhansky–Muller incompatibilities) but also maladaptation, both expected to be most pronounced in contact zones. In addition, embryo abortion might reflect physiological stress on females and embryos independent of any genetic stress. We examined all embryos of >500 females sampled outside and inside contact zones of three populations in Sweden. Females' clutch size ranged from 0 to 1,011 embryos (mean 130 ± 123), and abortion rates varied between 0% and 100% (mean 12%). We described female genotypes by using a hybrid index based on hundreds of SNPs differentiated between ecotypes with which we characterized female genotypes. We also calculated female SNP heterozygosity and inversion karyotype. Clutch size did not vary with female hybrid index, and abortion rates were only weakly related to hybrid index in two sites but not at all in a third site. No additional variation in abortion rate was explained by female SNP heterozygosity, but increased female inversion heterozygosity added slightly to increased abortion. Our results show only weak and probably biologically insignificant post‐zygotic barriers contributing to ecotype divergence, and the high and variable abortion rates were marginally, if at all, explained by hybrid index of females. AU - Johannesson, Kerstin AU - Zagrodzka, Zuzanna AU - Faria, Rui AU - Westram, Anja M AU - Butlin, Roger K. ID - 7205 IS - 3 JF - Journal of Evolutionary Biology SN - 1010061X TI - Is embryo abortion a post-zygotic barrier to gene flow between Littorina ecotypes? VL - 33 ER - TY - THES AB - This thesis concerns itself with the interactions of evolutionary and ecological forces and the consequences on genetic diversity and the ultimate survival of populations. It is important to understand what signals processes leave on the genome and what we can infer from such data, which is usually abundant but noisy. Furthermore, understanding how and when populations adapt or go extinct is important for practical purposes, such as the genetic management of populations, as well as for theoretical questions, since local adaptation can be the first step toward speciation. In Chapter 2, we introduce the method of maximum entropy to approximate the demographic changes of a population in a simple setting, namely the logistic growth model with immigration. We show that this method is not only a powerful tool in physics but can be gainfully applied in an ecological framework. We investigate how well it approximates the real behavior of the system, and find that is does so, even in unexpected situations. Finally, we illustrate how it can model changing environments. In Chapter 3, we analyze the co-evolution of allele frequencies and population sizes in an infinite island model. We give conditions under which polygenic adaptation to a rare habitat is possible. The model we use is based on the diffusion approximation, considers eco-evolutionary feedback mechanisms (hard selection), and treats both drift and environmental fluctuations explicitly. We also look at limiting scenarios, for which we derive analytical expressions. In Chapter 4, we present a coalescent based simulation tool to obtain patterns of diversity in a spatially explicit subdivided population, in which the demographic history of each subpopulation can be specified. We compare the results to existing predictions, and explore the relative importance of time and space under a variety of spatial arrangements and demographic histories, such as expansion and extinction. In the last chapter, we give a brief outlook to further research. AU - Szep, Eniko ID - 8574 TI - Local adaptation in metapopulations ER - TY - DATA AB - Here are the research data underlying the publication "Estimating inbreeding and its effects in a long-term study of snapdragons (Antirrhinum majus)". Further information are summed up in the README document. The files for this record have been updated and are now found in the linked DOI https://doi.org/10.15479/AT:ISTA:9192. AU - Arathoon, Louise S ID - 8254 TI - Estimating inbreeding and its effects in a long-term study of snapdragons (Antirrhinum majus) ER - TY - GEN AB - More than 100 years after Grigg’s influential analysis of species’ borders, the causes of limits to species’ ranges still represent a puzzle that has never been understood with clarity. The topic has become especially important recently as many scientists have become interested in the potential for species’ ranges to shift in response to climate change—and yet nearly all of those studies fail to recognise or incorporate evolutionary genetics in a way that relates to theoretical developments. I show that range margins can be understood based on just two measurable parameters: (i) the fitness cost of dispersal—a measure of environmental heterogeneity—and (ii) the strength of genetic drift, which reduces genetic diversity. Together, these two parameters define an ‘expansion threshold’: adaptation fails when genetic drift reduces genetic diversity below that required for adaptation to a heterogeneous environment. When the key parameters drop below this expansion threshold locally, a sharp range margin forms. When they drop below this threshold throughout the species’ range, adaptation collapses everywhere, resulting in either extinction or formation of a fragmented metapopulation. Because the effects of dispersal differ fundamentally with dimension, the second parameter—the strength of genetic drift—is qualitatively different compared to a linear habitat. In two-dimensional habitats, genetic drift becomes effectively independent of selection. It decreases with ‘neighbourhood size’—the number of individuals accessible by dispersal within one generation. Moreover, in contrast to earlier predictions, which neglected evolution of genetic variance and/or stochasticity in two dimensions, dispersal into small marginal populations aids adaptation. This is because the reduction of both genetic and demographic stochasticity has a stronger effect than the cost of dispersal through increased maladaptation. The expansion threshold thus provides a novel, theoretically justified, and testable prediction for formation of the range margin and collapse of the species’ range. AU - Polechova, Jitka ID - 9839 TI - Data from: Is the sky the limit? On the expansion threshold of a species' range ER - TY - JOUR AB - Empirical data suggest that inversions in many species contain genes important for intraspecific divergence and speciation, yet mechanisms of evolution remain unclear. While genes inside an inversion are tightly linked, inversions are not static but evolve separately from the rest of the genome by new mutations, recombination within arrangements, and gene flux between arrangements. Inversion polymorphisms are maintained by different processes, for example, divergent or balancing selection, or a mix of multiple processes. Moreover, the relative roles of selection, drift, mutation, and recombination will change over the lifetime of an inversion and within its area of distribution. We believe inversions are central to the evolution of many species, but we need many more data and new models to understand the complex mechanisms involved. AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger K. AU - Westram, Anja M ID - 5911 IS - 3 JF - Trends in Ecology and Evolution SN - 01695347 TI - Evolving inversions VL - 34 ER - TY - JOUR AB - Pollinators display a remarkable diversity of foraging strategies with flowering plants, from primarily mutualistic interactions to cheating through nectar robbery. Despite numerous studies on the effect of nectar robbing on components of plant fitness, its contribution to reproductive isolation is unclear. We experimentally tested the impact of different pollinator strategies in a natural hybrid zone between two subspecies of Antirrhinum majus with alternate flower colour guides. On either side of a steep cline in flower colour between Antirrhinum majus pseudomajus (magenta) and A. m. striatum (yellow), we quantified the behaviour of all floral visitors at different time points during the flowering season. Using long-run camera surveys, we quantify the impact of nectar robbing on the number of flowers visited per inflorescence and the flower probing time. We further experimentally tested the effect of nectar robbing on female reproductive success by manipulating the intensity of robbing. While robbing increased over time the number of legitimate visitors tended to decrease concomitantly. We found that the number of flowers pollinated on a focal inflorescence decreased with the number of prior robbing events. However, in the manipulative experiment, fruit set and fruit volume did not vary significantly between low robbing and control treatments. Our findings challenge the idea that robbers have a negative impact on plant fitness through female function. This study also adds to our understanding of the components of pollinator-mediated reproductive isolation and the maintenance of Antirrhinum hybrid zones. AU - Andalo, Christophe AU - Burrus, Monique AU - Paute, Sandrine AU - Lauzeral, Christine AU - Field, David ID - 5680 IS - 1 JF - Botany Letters SN - 23818107 TI - Prevalence of legitimate pollinators and nectar robbers and the consequences for fruit set in an Antirrhinum majus hybrid zone VL - 166 ER - TY - JOUR AB - The evolution of new species is made easier when traits under divergent ecological selection are also mating cues. Such ecological mating cues are now considered more common than previously thought, but we still know little about the genetic changes underlying their evolution or more generally about the genetic basis for assortative mating behaviors. Both tight physical linkage and the existence of large-effect preference loci will strengthen genetic associations between behavioral and ecological barriers, promoting the evolution of assortative mating. The warning patterns of Heliconius melpomene and H. cydno are under disruptive selection due to increased predation of nonmimetic hybrids and are used during mate recognition. We carried out a genome-wide quantitative trait locus (QTL) analysis of preference behaviors between these species and showed that divergent male preference has a simple genetic basis. We identify three QTLs that together explain a large proportion (approximately 60%) of the difference in preference behavior observed between the parental species. One of these QTLs is just 1.2 (0-4.8) centiMorgans (cM) from the major color pattern gene optix, and, individually, all three have a large effect on the preference phenotype. Genomic divergence between H. cydno and H. melpomene is high but broadly heterogenous, and admixture is reduced at the preference-optix color pattern locus but not the other preference QTLs. The simple genetic architecture we reveal will facilitate the evolution and maintenance of new species despite ongoing gene flow by coupling behavioral and ecological aspects of reproductive isolation. AU - Merrill, Richard M. AU - Rastas, Pasi AU - Martin, Simon H. AU - Melo Hurtado, Maria C AU - Barker, Sarah AU - Davey, John AU - Mcmillan, W. Owen AU - Jiggins, Chris D. ID - 6022 IS - 2 JF - PLoS Biology TI - Genetic dissection of assortative mating behavior VL - 17 ER - TY - GEN AU - Merrill, Richard M. AU - Rastas, Pasi AU - Martin, Simon H. AU - Melo Hurtado, Maria C AU - Barker, Sarah AU - Davey, John AU - Mcmillan, W. Owen AU - Jiggins, Chris D. ID - 9801 TI - Raw behavioral data ER - TY - JOUR AB - Both classical and recent studies suggest that chromosomal inversion polymorphisms are important in adaptation and speciation. However, biases in discovery and reporting of inversions make it difficult to assess their prevalence and biological importance. Here, we use an approach based on linkage disequilibrium among markers genotyped for samples collected across a transect between contrasting habitats to detect chromosomal rearrangements de novo. We report 17 polymorphic rearrangements in a single locality for the coastal marine snail, Littorina saxatilis. Patterns of diversity in the field and of recombination in controlled crosses provide strong evidence that at least the majority of these rearrangements are inversions. Most show clinal changes in frequency between habitats, suggestive of divergent selection, but only one appears to be fixed for different arrangements in the two habitats. Consistent with widespread evidence for balancing selection on inversion polymorphisms, we argue that a combination of heterosis and divergent selection can explain the observed patterns and should be considered in other systems spanning environmental gradients. AU - Faria, Rui AU - Chaube, Pragya AU - Morales, Hernán E. AU - Larsson, Tomas AU - Lemmon, Alan R. AU - Lemmon, Emily M. AU - Rafajlović, Marina AU - Panova, Marina AU - Ravinet, Mark AU - Johannesson, Kerstin AU - Westram, Anja M AU - Butlin, Roger K. ID - 6095 IS - 6 JF - Molecular Ecology SN - 0962-1083 TI - Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilis ecotypes VL - 28 ER - TY - JOUR AB - Great care is needed when interpreting claims about the genetic basis of human variation based on data from genome-wide association studies. AU - Barton, Nicholas H AU - Hermisson, Joachim AU - Nordborg, Magnus ID - 6230 JF - eLife TI - Why structure matters VL - 8 ER - TY - JOUR AB - One of the most striking and consistent results in speciation genomics is the heterogeneous divergence observed across the genomes of closely related species. This pattern was initially attributed to different levels of gene exchange—with divergence preserved at loci generating a barrier to gene flow but homogenized at unlinked neutral loci. Although there is evidence to support this model, it is now recognized that interpreting patterns of divergence across genomes is not so straightforward. One problem is that heterogenous divergence between populations can also be generated by other processes (e.g. recurrent selective sweeps or background selection) without any involvement of differential gene flow. Thus, integrated studies that identify which loci are likely subject to divergent selection are required to shed light on the interplay between selection and gene flow during the early phases of speciation. In this issue of Molecular Ecology, Rifkin et al. (2019) confront this challenge using a pair of sister morning glory species. They wisely design their sampling to take the geographic context of individuals into account, including geographically isolated (allopatric) and co‐occurring (sympatric) populations. This enabled them to show that individuals are phenotypically less differentiated in sympatry. They also found that the loci that resist introgression are enriched for those most differentiated in allopatry and loci that exhibit signals of divergent selection. One great strength of the study is the combination of methods from population genetics and molecular evolution, including the development of a model to simultaneously infer admixture proportions and selfing rates. AU - Field, David AU - Fraisse, Christelle ID - 6466 IS - 7 JF - Molecular ecology TI - Breaking down barriers in morning glories VL - 28 ER - TY - JOUR AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA (small nucleolar RNA). Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 6467 IS - 4 JF - Biology Letters SN - 17449561 TI - The distribution of epistasis on simple fitness landscapes VL - 15 ER - TY - JOUR AB - The environment changes constantly at various time scales and, in order to survive, species need to keep adapting. Whether these species succeed in avoiding extinction is a major evolutionary question. Using a multilocus evolutionary model of a mutation‐limited population adapting under strong selection, we investigate the effects of the frequency of environmental fluctuations on adaptation. Our results rely on an “adaptive‐walk” approximation and use mathematical methods from evolutionary computation theory to investigate the interplay between fluctuation frequency, the similarity of environments, and the number of loci contributing to adaptation. First, we assume a linear additive fitness function, but later generalize our results to include several types of epistasis. We show that frequent environmental changes prevent populations from reaching a fitness peak, but they may also prevent the large fitness loss that occurs after a single environmental change. Thus, the population can survive, although not thrive, in a wide range of conditions. Furthermore, we show that in a frequently changing environment, the similarity of threats that a population faces affects the level of adaptation that it is able to achieve. We check and supplement our analytical results with simulations. AU - Trubenova, Barbora AU - Krejca, Martin AU - Lehre, Per Kristian AU - Kötzing, Timo ID - 6637 IS - 7 JF - Evolution TI - Surfing on the seascape: Adaptation in a changing environment VL - 73 ER - TY - JOUR AB - This paper analyzes how partial selfing in a large source population influences its ability to colonize a new habitat via the introduction of a few founder individuals. Founders experience inbreeding depression due to partially recessive deleterious alleles as well as maladaptation to the new environment due to selection on a large number of additive loci. I first introduce a simplified version of the Inbreeding History Model (Kelly, 2007) in order to characterize mutation‐selection balance in a large, partially selfing source population under selection involving multiple non‐identical loci. I then use individual‐based simulations to study the eco‐evolutionary dynamics of founders establishing in the new habitat under a model of hard selection. The study explores how selfing rate shapes establishment probabilities of founders via effects on both inbreeding depression and adaptability to the new environment, and also distinguishes the effects of selfing on the initial fitness of founders from its effects on the long‐term adaptive response of the populations they found. A high rate of (but not complete) selfing is found to aid establishment over a wide range of parameters, even in the absence of mate limitation. The sensitivity of the results to assumptions about the nature of polygenic selection are discussed. AU - Sachdeva, Himani ID - 6680 IS - 9 JF - Evolution SN - 0014-3820 TI - Effect of partial selfing and polygenic selection on establishment in a new habitat VL - 73 ER - TY - GEN AB - Evolutionary studies are often limited by missing data that are critical to understanding the history of selection. Selection experiments, which reproduce rapid evolution under controlled conditions, are excellent tools to study how genomes evolve under selection. Here we present a genomic dissection of the Longshanks selection experiment, in which mice were selectively bred over 20 generations for longer tibiae relative to body mass, resulting in 13% longer tibiae in two replicates. We synthesized evolutionary theory, genome sequences and molecular genetics to understand the selection response and found that it involved both polygenic adaptation and discrete loci of major effect, with the strongest loci tending to be selected in parallel between replicates. We show that selection may favor de-repression of bone growth through inactivating two limb enhancers of an inhibitor, Nkx3-2. Our integrative genomic analyses thus show that it is possible to connect individual base-pair changes to the overall selection response. AU - Castro, João Pl AU - Yancoskie, Michelle N. AU - Marchini, Marta AU - Belohlavy, Stefanie AU - Hiramatsu, Layla AU - Kučka, Marek AU - Beluch, William H. AU - Naumann, Ronald AU - Skuplik, Isabella AU - Cobb, John AU - Barton, Nicholas H AU - Rolian, Campbell AU - Chan, Yingguang Frank ID - 9804 TI - Data from: An integrative genomic analysis of the Longshanks selection experiment for longer limbs in mice ER - TY - GEN AB - This paper analyzes how partial selfing in a large source population influences its ability to colonize a new habitat via the introduction of a few founder individuals. Founders experience inbreeding depression due to partially recessive deleterious alleles as well as maladaptation to the new environment due to selection on a large number of additive loci. I first introduce a simplified version of the Inbreeding History Model (Kelly, 2007) in order to characterize mutation-selection balance in a large, partially selfing source population under selection involving multiple non-identical loci. I then use individual-based simulations to study the eco-evolutionary dynamics of founders establishing in the new habitat under a model of hard selection. The study explores how selfing rate shapes establishment probabilities of founders via effects on both inbreeding depression and adaptability to the new environment, and also distinguishes the effects of selfing on the initial fitness of founders from its effects on the long-term adaptive response of the populations they found. A high rate of (but not complete) selfing is found to aid establishment over a wide range of parameters, even in the absence of mate limitation. The sensitivity of the results to assumptions about the nature of polygenic selection are discussed. AU - Sachdeva, Himani ID - 9802 TI - Data from: Effect of partial selfing and polygenic selection on establishment in a new habitat ER - TY - JOUR AB - The green‐beard effect is one proposed mechanism predicted to underpin the evolu‐tion of altruistic behavior. It relies on the recognition and the selective help of altruists to each other in order to promote and sustain altruistic behavior. However, this mechanism has often been dismissed as unlikely or uncommon, as it is assumed that both the signaling trait and altruistic trait need to be encoded by the same gene or through tightly linked genes. Here, we use models of indirect genetic effects (IGEs) to find the minimum correlation between the signaling and altruistic trait required for the evolution of the latter. We show that this correlation threshold depends on the strength of the interaction (influence of the green beard on the expression of the altruistic trait), as well as the costs and benefits of the altruistic behavior. We further show that this correlation does not necessarily have to be high and support our analytical results by simulations. AU - Trubenova, Barbora AU - Hager, Reinmar ID - 6795 IS - 17 JF - Ecology and Evolution TI - Green beards in the light of indirect genetic effects VL - 9 ER - TY - JOUR AB - * Understanding the mechanisms causing phenotypic differences between females and males has long fascinated evolutionary biologists. An extensive literature exists on animal sexual dimorphism but less information is known about sex differences in plants, particularly the extent of geographical variation in sexual dimorphism and its life‐cycle dynamics. * Here, we investigated patterns of genetically based sexual dimorphism in vegetative and reproductive traits of a wind‐pollinated dioecious plant, Rumex hastatulus, across three life‐cycle stages using open‐pollinated families from 30 populations spanning the geographic range and chromosomal variation (XY and XY1Y2) of the species. * The direction and degree of sexual dimorphism was highly variable among populations and life‐cycle stages. Sex‐specific differences in reproductive function explained a significant amount of temporal change in sexual dimorphism. For several traits, geographical variation in sexual dimorphism was associated with bioclimatic parameters, likely due to the differential responses of the sexes to climate. We found no systematic differences in sexual dimorphism between chromosome races. * Sex‐specific trait differences in dioecious plants largely result from a balance between sexual and natural selection on resource allocation. Our results indicate that abiotic factors associated with geographical context also play a role in modifying sexual dimorphism during the plant life‐cycle. AU - Puixeu Sala, Gemma AU - Pickup, Melinda AU - Field, David AU - Barrett, Spencer C.H. ID - 6831 IS - 3 JF - New Phytologist TI - Variation in sexual dimorphism in a wind-pollinated plant: The influence of geographical context and life-cycle dynamics VL - 224 ER - TY - GEN AB - Understanding the mechanisms causing phenotypic differences between females and males has long fascinated evolutionary biologists. An extensive literature exists on animal sexual dimorphism but less is known about sex differences in plants, particularly the extent of geographical variation in sexual dimorphism and its life-cycle dynamics. Here, we investigate patterns of genetically-based sexual dimorphism in vegetative and reproductive traits of a wind-pollinated dioecious plant, Rumex hastatulus, across three life-cycle stages using open-pollinated families from 30 populations spanning the geographic range and chromosomal variation (XY and XY1Y2) of the species. The direction and degree of sexual dimorphism was highly variable among populations and life-cycle stages. Sex-specific differences in reproductive function explained a significant amount of temporal change in sexual dimorphism. For several traits, geographical variation in sexual dimorphism was associated with bioclimatic parameters, likely due to the differential responses of the sexes to climate. We found no systematic differences in sexual dimorphism between chromosome races. Sex-specific trait differences in dioecious plants largely result from a balance between sexual and natural selection on resource allocation. Our results indicate that abiotic factors associated with geographical context also play a role in modifying sexual dimorphism during the plant life cycle. AU - Puixeu Sala, Gemma AU - Pickup, Melinda AU - Field, David AU - Barrett, Spencer C.H. ID - 9803 TI - Data from: Variation in sexual dimorphism in a wind-pollinated plant: the influence of geographical context and life-cycle dynamics ER - TY - JOUR AB - Many traits of interest are highly heritable and genetically complex, meaning that much of the variation they exhibit arises from differences at numerous loci in the genome. Complex traits and their evolution have been studied for more than a century, but only in the last decade have genome-wide association studies (GWASs) in humans begun to reveal their genetic basis. Here, we bring these threads of research together to ask how findings from GWASs can further our understanding of the processes that give rise to heritable variation in complex traits and of the genetic basis of complex trait evolution in response to changing selection pressures (i.e., of polygenic adaptation). Conversely, we ask how evolutionary thinking helps us to interpret findings from GWASs and informs related efforts of practical importance. AU - Sella, Guy AU - Barton, Nicholas H ID - 6855 JF - Annual Review of Genomics and Human Genetics SN - 1527-8204 TI - Thinking about the evolution of complex traits in the era of genome-wide association studies VL - 20 ER -