@article{21759, abstract = {Promoters and enhancers are cis-regulatory elements (CREs), DNA sequences that bind transcription factor (TF) proteins to up- or down-regulate target genes. Decades-long efforts yielded TF-DNA interaction models that predict how strongly an individual TF binds arbitrary DNA sequences and how individual binding events on the CRE combine to affect gene expression. These insights can be synthesized into a global, biophysically realistic, and quantitative genotype-phenotype (GP) map for gene regulation, a ‘holy grail’ for the application of evolutionary theory. A global map provides a rare opportunity to simulate the long-term evolution of regulatory sequences and pose several fundamental questions: How long does it take to evolve CREs de novo? How many non-trivial regulatory functions exist in sequence space? How connected are they? For which regulatory architecture is CRE evolution most rapid and evolvable? In this article, the second of a two-part series, we review the application of evolutionary concepts — epistasis, robustness, evolvability, tunability, plasticity, and bet-hedging — to the evolution of gene regulatory sequences. We then evaluate the potential for a unifying theory for the evolution of regulatory sequences and identify key open challenges.}, author = {Mascolo, Elia and Körei, Reka E and Borst, Noa O. and Barton, Nicholas H and Crocker, Justin and Tkačik, Gašper}, issn = {1879-0380}, journal = {Current Opinion in Genetics and Development}, publisher = {Elsevier}, title = {{Long-term evolution of regulatory DNA sequences. Part 2: Theory and future challenges}}, doi = {10.1016/j.gde.2026.102472}, volume = {98}, year = {2026}, } @article{21841, abstract = {The long-standing notion that genotypes map to phenotypes through simple one gene–one trait relationships continues to shape both research in the life sciences and public understanding, with implications for policy and funding priorities. Yet this paradigm is increasingly recognized as inadequate for explaining continuous phenotypic variation and the complex genetic architectures of the genotype–phenotype map. Modern genetics emerged from the early 20th-century synthesis of Mendelian and biometric schools of heredity, with R.A. Fisher demonstrating early on how multiple discrete loci could collectively produce continuous variation. Despite this fundamental insight, Mendelism—with its focus on single genes and standardized genetic backgrounds—became the dominant framework, shaping current genetics research and molecular biology as well as science education. The advent of large-scale genomic data has revealed yet again the limitations of this reductionist approach. Evidence from quantitative genetics now shows that most phenotypes arise from complex networks of many interdependent genes and their dynamic responses to environmental perturbations. Here we trace the historical roots of how Mendelian classical genetics departed from the biometric school to create the current predominant paradigm in genetics, despite fundamentally unresolved issues. Moving on from this one-sided paradigm will require systematic development of integrative, evolutionarily grounded experimental approaches that better capture the multigenic and context-dependent nature of inheritance. Achieving such an extended perspective will require methodological innovation, including advances in large-scale (e.g. automated) phenotyping. Dedicated research programs will be necessary to advance a new era of genetic research into the complex mechanisms underlying phenotypic variation.}, author = {Tautz, Diethard and Pallares, Luisa F and Andersson, Leif and Barghi, Neda and Barton, Nicholas H and Bay, Rachael and Chan, Yingguang Frank and Hancock, Angela and Kaiser, Tobias S and Koenig, Daniel and Kontarakis, Zacharias and Liedvogel, Miriam and de Meaux, Juliette and Nordborg, Magnus and Palmer, Abraham A and Purugganan, Michael and Schlötterer, Christian and Schmid, Karl and Stainier, Didier Y R and Weigel, Detlef and Wolf, Jochen B W and Ebert, Dieter and Gibson, Greg}, issn = {1943-2631}, journal = {Genetics}, keywords = {classic genetics, quantitative genetics, genotype–phenotype map}, number = {4}, publisher = {Oxford University Press}, title = {{Beyond Mendel: A call to revisit the genotype–phenotype map through new experimental paradigms}}, doi = {10.1093/genetics/iyag024}, volume = {232}, year = {2026}, } @unpublished{21968, abstract = {Balancing selection, a form of selection that maintains genetic diversity, is difficult to detect, and the importance of balancing selection for the maintenance of genetic variation may be larger than often assumed. We model the possibility that the diversity-promoting effects of balancing selection extend to other loci that show sign epistasis with a locus under balancing selection. Rather than focusing on overdominance, as was done in previous efforts, we explore the effects of negative frequency dependence and show that this has important effects on the conditions under which the diversity-promoting effect of epistasis can occur in diploids. Our results show that not only recombination rate but also the dominance of sign epistasis are key parameters that determine the maintenance of polymorphism beyond the locus under direct balancing selection. We suggest that the effect we explore may play a significant role, especially when balancing selection acts on major effect loci.}, author = {Khudiakova, Kseniia and Barton, Nicholas H and Arnqvist, Goran}, booktitle = {bioRxiv}, title = {{Sign epistasis extends the effects of balancing selection on genetic diversity}}, doi = {10.1101/2025.04.09.647826}, year = {2026}, } @article{20325, abstract = {Inferring genealogical relationships of wild populations is useful because it gives direct estimates of mating patterns and variance in reproductive success. Inference can be improved by including information about parentage shared between siblings, or by modelling phenotypes or population data related to mating. However, we currently lack a framework to infer parent–offspring relationships, sibships and population parameters in a single analysis. To address this, we here extend a previous method, Fractional Analysis of Paternity and Sibships, to include population data for the case where one parent is known. We illustrate this with the example of pollen dispersal in a natural hybrid zone population of the snapdragon Antirrhinum majus. Pollen dispersal is leptokurtic, with half of mating events occurring within 30 m, but with a long tail of mating events up to 859 m. Using simulations, we find that both sibship and population information substantially improve pedigree reconstruction, and that we can expect to resolve median dispersal distances with high accuracy.}, author = {Ellis, Thomas and Field, David and Barton, Nicholas H}, issn = {1365-294X}, journal = {Molecular Ecology}, number = {15}, publisher = {Wiley}, title = {{Joint estimation of paternity, sibships and pollen dispersal in a snapdragon hybrid zone}}, doi = {10.1111/mec.70051}, volume = {34}, year = {2025}, } @article{20190, abstract = {A major goal of speciation research is identifying loci that underpin barriers to gene flow. Population genomics takes a ‘bottom-up’ approach, scanning the genome for molecular signatures of processes that drive or maintain divergence. However, interpreting the ‘genomic landscape’ of speciation is complicated, because genome scans conflate multiple processes, most of which are not informative about gene flow. However, studying replicated population contrasts, including multiple incidences of secondary contact, can strengthen inferences. In this paper, we use linked-read sequencing (haplotagging), FST scans and genealogical methods to characterise the genomic landscape associated with replicate hybrid zone formation. We studied two flower colour varieties of the common snapdragon, Antirrhinum majus subspecies majus, that form secondary hybrid zones in multiple independent valleys in the Pyrenees. Consistent with past work, we found very low differentiation at one well-studied zone (Planoles). However, at a second zone (Avellanet), we found stronger differentiation and greater heterogeneity, which we argue is due to differences in the amount of introgression following secondary contact. Topology weighting of genealogical trees identified loci where haplotype diversity was associated with the two snapdragon varieties. Two of the strongest associations were at previously identified flower colour loci: Flavia, that affects yellow pigmentation, and Rosea/Eluta, two linked loci that affect magenta pigmentation. Preliminary analysis of coalescence times provides additional evidence for selective sweeps at these loci and barriers to gene flow. Our study highlights the impact of demographic history on the differentiation landscape, emphasising the need to distinguish between historical divergence and recent introgression.}, author = {Pal, Arka and Shipilina, Daria and Le Moan, Alan and Mcnairn, Adrian J. and Grenier, Jennifer K. and Kucka, Marek and Coop, Graham and Chan, Yingguang Frank and Barton, Nicholas H and Field, David and Stankowski, Sean}, issn = {1365-294X}, journal = {Molecular Ecology}, number = {22}, publisher = {Wiley}, title = {{Genealogical analysis of replicate flower colour hybrid zones in Antirrhinum}}, doi = {10.1111/mec.70067}, volume = {34}, year = {2025}, } @article{17888, abstract = {Context: Biotic resource exploitation is a critical determinant of species’ distributions. However, quantifying resource exploitation patterns through space and time can be difficult, complicating their incorporation in spatial ecology studies. Therefore, understanding the local drivers of spatial patterns of resource exploitation may contribute to better large-scale species distribution models. Objectives: We investigated (1) how the resource exploitation patterns of two trophic interactions (plant–insect) are explained by insect behaviour, resource aggregation, and potential insect-insect interactions. We also analyzed how (2) resource patch size and (3) resource accessibility in a heterogeneous landscape affected host exploitation patterns. Methods: We quantified nectar robbing by insects in the genus Bombus (bumblebees) and seed predation by Brachypterolus vestitus larvae (Antirrhinum beetle) on Antirrhinum majus L. (wild snapdragons) in the Pyrenees Mountains, Catalonia, Spain. We tested hypotheses about resource exploitation by integrating spatial analyses at multiple scales. Results: Both trophic interactions were aggregated, explained by the aggregation of their resource. At some scales, nectar robbing is more aggregated than the resource. Trophic interaction abundance is proportional to resource patch size, following the ideal free distribution model. Landscape features do not explain the locations exploited. Nectar robbing and seed predation occur together more often than expected. Conclusions: Our findings suggest that multiple biotic and ecological spatial factors may simultaneously affect resource exploitation at a local scale. These findings should be considered when developing agricultural projects, management plans and conservation policies.}, author = {Pocull Belles, Guillem and Baskett, Carina and Barton, Nicholas H}, issn = {1572-9761}, journal = {Landscape Ecology}, number = {9}, publisher = {Springer Nature}, title = {{Multiscale spatial analysis of two plant–insect interactions: Effects of landscape, resource distribution, and other insects}}, doi = {10.1007/s10980-024-01899-9}, volume = {39}, year = {2024}, } @article{18949, abstract = {Speciation research—the scientific field focused on understanding the origin and diversity of species—has a long and complex history. While relevant to one another, the specific goals and activities of speciation researchers are highly diverse, and scattered across a collection of different perspectives. Thus, our understanding of speciation will benefit from efforts to bridge scientific findings and the diverse people who do the work. In this paper, we outline two ways of integrating speciation research: (i) scientific integration, through the bringing together of ideas, data, and approaches; and (ii) social integration, by creating ways for a diversity of researchers to participate in the scientific process. We then discuss five challenges to integration: (i) the multidisciplinary nature of speciation research, (ii) the complex language of speciation; (iii) a bias toward certain study systems; (iv) the challenges of working across scales; and (v) inconsistent measures and reporting standards. We provide practical steps that individuals and groups can take to help overcome these challenges, and argue that integration is a team effort in which we all have a role to play.}, author = {Stankowski, Sean and Cutter, Asher D and Satokangas, Ina and Lerch, Brian A and Rolland, Jonathan and Smadja, Carole M and Segami Marzal, J Carolina and Cooney, Christopher R and Feulner, Philine G D and Domingos, Fabricius Maia Chaves Bicalho and North, Henry L and Yamaguchi, Ryo and Butlin, Roger K and Wolf, Jochen B W and Coughlan, Jenn and Heidbreder, Patrick and Hernández-Gutiérrez, Rebeca and Barnard-Kubow, Karen B and Peede, David and Rancilhac, Loïs and Salvador, Rodrigo Brincalepe and Thompson, Ken A and Stacy, Elizabeth A and Moyle, Leonie C and Garlovsky, Martin D and Maulana, Arif and Kantelinen, Annina and Cacho, N Ivalú and Schneemann, Hilde and Domínguez, Marisol and Dopman, Erik B and Lohse, Konrad and Rometsch, Sina J and Comeault, Aaron A and Merrill, Richard M and Scordato, Elizabeth S C and Singhal, Sonal and Pärssinen, Varpu and Lackey, Alycia C R and Kumar, Sanghamitra and Meier, Joana I and Barton, Nicholas H and Fraisse, Christelle and Ravinet, Mark and Kulmuni, Jonna}, issn = {2752-938X}, journal = {Evolutionary Journal of the Linnean Society}, number = {1}, publisher = {Oxford University Press}, title = {{Toward the integration of speciation research}}, doi = {10.1093/evolinnean/kzae001}, volume = {3}, year = {2024}, } @article{15358, abstract = {We consider how a population of N haploid individuals responds to directional selection on standing variation, with no new variation from recombination or mutation. Individuals have trait values z1,…,zN, which are drawn from a distribution ψ; the fitness of individual i is proportional to [Formula: see text] . For illustration, we consider the Laplace and Gaussian distributions, which are parametrised only by the variance V0, and show that for large N, there is a scaling limit which depends on a single parameter NV0. When selection is weak relative to drift (NV0≪1), the variance decreases exponentially at rate 1/N, and the expected ultimate gain in log fitness (scaled by V0), is just NV0, which is the same as Robertson's (1960) prediction for a sexual population. In contrast, when selection is strong relative to drift (NV0≫1), the ultimate gain can be found by approximating the establishment of alleles by a branching process in which each allele competes independently with the population mean and the fittest allele to establish is certain to fix. Then, if the probability of survival to time t∼1/V0 of an allele with value z is P(z), with mean P¯, the winning allele is the fittest of NP¯ survivors drawn from a distribution ψP/P¯. The expected ultimate change is ∼2log(1.15NV0) for a Gaussian distribution, and ∼-12log0.36NV0-log-log0.36NV0 for a Laplace distribution. This approach also predicts the variability of the process, and its dynamics; we show that in the strong selection regime, the expected genetic variance decreases as ∼t-3 at large times. We discuss how these results may be related to selection on standing variation that is spread along a linear chromosome.}, author = {Barton, Nicholas H and Sachdeva, Himani}, issn = {1096-0325}, journal = {Theoretical Population Biology}, pages = {129--137}, publisher = {Elsevier}, title = {{Limits to selection on standing variation in an asexual population}}, doi = {10.1016/j.tpb.2024.04.001}, volume = {157}, year = {2024}, } @article{17238, abstract = {We know that heritable variation is abundant, and that selection causes all but the smallest populations to rapidly shift beyond their original trait distribution. So then, what limits the range of a species? There are physical constraints and also population genetic limits to the effectiveness of selection, ultimately set by population size. Global adaptation, where the same genotype is favoured over the whole range, is most efficient when based on a multitude of weakly selected alleles and is effective even when local demes are small, provided that there is some gene flow. In contrast, local adaptation is sensitive to gene flow and may require alleles with substantial effect. How can populations combine the advantages of large effective size with the ability to specialise into local niches? To what extent does reproductive isolation help resolve this tension? I address these questions using eco-evolutionary models of polygenic adaptation, contrasting discrete demes with continuousspace.}, author = {Barton, Nicholas H}, issn = {1420-9101}, journal = {Journal of Evolutionary Biology}, number = {6}, pages = {605--615}, publisher = {Oxford University Press}, title = {{Limits to species' range: The tension between local and global adaptation}}, doi = {10.1093/jeb/voae052}, volume = {37}, year = {2024}, } @article{18491, abstract = {Predicting the outcomes of adaptation is a major goal of evolutionary biology. When temporal changes in the environment mirror spatial gradients, it opens up the potential for predicting the course of adaptive evolution over time based on patterns of spatial genetic and phenotypic variation. We assessed this approach in a 30-year transplant experiment in the intertidal snail Littorina saxatilis. In 1992, snails were transplanted from a predation-dominated environment to one dominated by wave action. On the basis of spatial patterns, we predicted transitions in shell size and morphology, allele frequencies at positions throughout the genome, and chromosomal rearrangement frequencies. Observed changes closely agreed with predictions and transformation was both dramatic and rapid. Hence, adaptation can be predicted from knowledge of the phenotypic and genetic variation among populations.}, author = {Garcia Castillo, Diego Fernando and Barton, Nicholas H and Faria, Rui and Larsson, Jenny and Stankowski, Sean and Butlin, Roger and Johannesson, Kerstin and Westram, Anja M}, issn = {2375-2548}, journal = {Science Advances}, number = {41}, publisher = {AAAS}, title = {{Predicting rapid adaptation in time from adaptation in space: A 30-year field experiment in marine snails}}, doi = {10.1126/sciadv.adp2102}, volume = {10}, year = {2024}, } @misc{18498, abstract = {Scripts and data used in the research study Predicting rapid adaptation in time from adaptation in space: a 30-year field experiment in marine snails. https://doi.org/10.1101/2023.09.27.559715}, author = {Garcia Castillo, Diego Fernando and Barton, Nicholas H and Faria, Rui and Larsson, Jenny and Stankowski, Sean and Butlin, Roger and Johannesson, Kerstin and Westram, Anja M}, publisher = {Zenodo}, title = {{Data and code for: Predicting rapid adaptation in time from adaptation in space: a 30-year field experiment in marine snails}}, doi = {10.5281/ZENODO.12159343}, year = {2024}, } @article{14452, abstract = {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.}, author = {Barton, Nicholas H and Etheridge, Alison M. and Véber, Amandine}, issn = {1943-2631}, journal = {Genetics}, number = {2}, publisher = {Oxford University Press}, title = {{The infinitesimal model with dominance}}, doi = {10.1093/genetics/iyad133}, volume = {225}, year = {2023}, } @article{14556, abstract = {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.}, author = {Berdan, Emma L. and Barton, Nicholas H and Butlin, Roger and Charlesworth, Brian and Faria, Rui and Fragata, Inês and Gilbert, Kimberly J. and Jay, Paul and Kapun, Martin and Lotterhos, Katie E. and Mérot, Claire and Durmaz Mitchell, Esra and Pascual, Marta and Peichel, Catherine L. and Rafajlović, Marina and Westram, Anja M and Schaeffer, Stephen W. and Johannesson, Kerstin and Flatt, Thomas}, issn = {1420-9101}, journal = {Journal of Evolutionary Biology}, number = {12}, publisher = {Wiley}, title = {{How chromosomal inversions reorient the evolutionary process}}, doi = {10.1111/jeb.14242}, volume = {36}, year = {2023}, } @misc{12949, abstract = {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.}, author = {Barton, Nicholas H}, keywords = {Quantitative genetics, infinitesimal model}, publisher = {Institute of Science and Technology Austria}, title = {{The infinitesimal model with dominance}}, doi = {10.15479/AT:ISTA:12949}, year = {2023}, } @article{12521, abstract = {Differentiated X chromosomes are expected to have higher rates of adaptive divergence than autosomes, if new beneficial mutations are recessive (the “faster-X effect”), largely because these mutations are immediately exposed to selection in males. The evolution of X chromosomes after they stop recombining in males, but before they become hemizygous, has not been well explored theoretically. We use the diffusion approximation to infer substitution rates of beneficial and deleterious mutations under such a scenario. Our results show that selection is less efficient on diploid X loci than on autosomal and hemizygous X loci under a wide range of parameters. This “slower-X” effect is stronger for genes affecting primarily (or only) male fitness, and for sexually antagonistic genes. These unusual dynamics suggest that some of the peculiar features of X chromosomes, such as the differential accumulation of genes with sex-specific functions, may start arising earlier than previously appreciated.}, author = {Mrnjavac, Andrea and Khudiakova, Kseniia and Barton, Nicholas H and Vicoso, Beatriz}, issn = {2056-3744}, journal = {Evolution Letters}, keywords = {Genetics, Ecology, Evolution, Behavior and Systematics}, number = {1}, publisher = {Oxford University Press}, title = {{Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution}}, doi = {10.1093/evlett/qrac004}, volume = {7}, year = {2023}, } @article{12159, abstract = {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.}, author = {Shipilina, Daria and Pal, Arka and Stankowski, Sean and Chan, Yingguang Frank and Barton, Nicholas H}, issn = {1365-294X}, journal = {Molecular Ecology}, keywords = {Genetics, Ecology, Evolution, Behavior and Systematics}, number = {6}, pages = {1441--1457}, publisher = {Wiley}, title = {{On the origin and structure of haplotype blocks}}, doi = {10.1111/mec.16793}, volume = {32}, year = {2023}, } @article{11546, abstract = {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.}, author = {Westram, Anja M and Faria, Rui and Johannesson, Kerstin and Butlin, Roger and Barton, Nicholas H}, issn = {1471-2970}, journal = {Philosophical Transactions of the Royal Society B: Biological Sciences}, keywords = {General Agricultural and Biological Sciences, General Biochemistry, Genetics and Molecular Biology}, number = {1856}, publisher = {Royal Society of London}, title = {{Inversions and parallel evolution}}, doi = {10.1098/rstb.2021.0203}, volume = {377}, year = {2022}, } @misc{11686, abstract = {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.}, author = {Turelli, Michael and Barton, Nicholas H}, keywords = {Biological sciences}, publisher = {Dryad}, title = {{Wolbachia frequency data from: Why did the Wolbachia transinfection cross the road? Drift, deterministic dynamics and disease control}}, doi = {10.25338/B81931}, year = {2022}, } @article{11702, abstract = {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.}, author = {Barton, Nicholas H}, issn = {1091-6490}, journal = {Proceedings of the National Academy of Sciences of the United States of America}, number = {30}, publisher = {National Academy of Sciences}, title = {{The "New Synthesis"}}, doi = {10.1073/pnas.2122147119}, volume = {119}, year = {2022}, } @article{12264, abstract = {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.}, author = {Westram, Anja M and Stankowski, Sean and Surendranadh, Parvathy and Barton, Nicholas H}, issn = {1420-9101}, journal = {Journal of Evolutionary Biology}, keywords = {Ecology, Evolution, Behavior and Systematics}, number = {9}, pages = {1143--1164}, publisher = {Wiley}, title = {{What is reproductive isolation?}}, doi = {10.1111/jeb.14005}, volume = {35}, year = {2022}, }