Effect of population structure on neutral genetic variation and barriers to gene exchange

Understanding the role of evolutionary processes in shaping genetic variation has been a primary goal in evolutionary genetics. In this regard, a key question is how genetically distinct populations evolve in the face of gene flow, thereby generating genetic and phenotypic divergence and reproductive isolation (RI). This requires quantifying the role and relative contributions of prezygotic and postzygotic isolating mechanisms on the reduction of gene exchange between populations, and identifying regions in the genome that mediate RI, which is often polygenic. Further, this needs distinguishing neutral and selected regions in the genome, and discerning how selection influences patterns of neutral divergence. Population structure, defined as any deviation from panmixia, such as geographic distribution, movement and mating patterns of individuals, influences how genetic variation is structured in space and shapes the neutral null model. Availability of large scale spatial genomic datasets now enables us to detect signatures of population structure in genetic data and infer population genetic parameters. Such inferences are crucial and have wide applications in biodiversity, conservation genetics, population management and medical genetics. However, inferences are based on assumptions that do not always match the complex reality, thus leading to erroneous conclusions. Moreover, the role and interaction of heterogeneous population density and dispersal, which are ubiquitous in nature, has been challenging to study owing to their mathematical complexity. In such scenarios, feedback between theory, data and simulations can prove to be useful. In this thesis, I examine the effect of population structure on neutral genetic variation and barriers to gene exchange in hybridising populations, thereby bridging together the fields of spatial population genetics and speciation. Despite being a key concept in speciation, reproductive isolation (RI) lacks a quantitative definition and has been used and measured differently across different fields. Chapter 2 gives a quantitative definition of RI, in terms of the effect of genetic differences on gene flow. We give analytical predictions for RI in a range of scenarios, in terms of effective migration rates for discrete populations and barrier strength for continuous populations. In addition to this, we discuss current measures of RI and their limitations, and propose the need for new measures that combine organismal and genetic perspectives of RI. In chapter 3, I examine the combined effect of assortative mating, sexual selection and viability selection on RI. For this, we consider a polygenic ‘magic’ trait under a mainland-island model. We obtain novel theoretical predictions for molecular divergence in terms of effective migration rates, which bears a simple relationship to measurable fitness components of migrants and various early generation hybrids. We explore the conditions under which local adaptation can be maintained despite maladaptive gene flow and quantify the relative contributions of viability and sexual selection to genome-wide barriers to gene flow. The next two chapters of the thesis focus on a hybrid zone of Antirrhinum majus that consist of two subspecies- the magenta flowered A. m. pseudomajus and the yellow flowered A.m. striatum. Previous studies have suggested that flower colour is target of pollinator mediated selection and is influenced only by few genes. While these regions show high genetic differentiation between the subspecies, the rest of the genome is seen to be well mixed. Chapter 4 examines the effects of heterogeneous population density and leptokurtic dispersal on isolation by distance and the distribution of heterozygosity by focusing on non-flower colour markers. Chapter 5 analyses cline shapes and associations among 6 focal flower colour markers to understand how selection and dispersal maintain this hybrid zone. We see sharp coincident stepped clines at all loci and positive associations throughout the hybrid zone, contrary to the expected patterns from diffusive gene flow. With a novel scheme of inferring dispersal combined with multilocus simulations, we show that stepped clines do not reflect genetic barriers to gene flow, but are rather a result of long-distance migration. This framework allows us to get realistic estimates gene flow and selection and shows how traditional cline analysis may lead to inaccurate conclusions when assumptions of the theory are not met. Overall, this thesis investigates how different features of population structure leave detectable signatures in genetic variation, namely in patterns of isolation by distance, linkage disequilibrium and genetic divergence. It also highlights how effective migration rates provide useful way of analysing polygenic architectures and shed new light into hybrid zones. In doing so, I identify scenarios when simple models become insufficient and suggest possibe directions by combining genetic data with simulations.