Analysis of spatial genetic variation reveals genetic divergence among populations of Primula veris associated to contrasting habitats

Pablo Deschepper,Hans Jacquemyn,Rein Brys,Miguel A Fortuna

doi:10.1038/s41598-017-09154-9

Pablo Deschepper, Hans Jacquemyn + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-09154-9

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Abstract

Genetic divergence by environment is a process whereby selection causes the formation of gene flow barriers between populations adapting to contrasting environments and is often considered to be the onset of speciation. Nevertheless, the extent to which genetic differentiation by environment on small spatial scales can be detected by means of neutral markers is still subject to debate. Previous research on the perennial herb Primula veris has shown that plants from grassland and forest habitats showed pronounced differences in phenology and flower morphology, suggesting limited gene flow between habitats. To test this hypothesis, we sampled 33 populations of P. veris consisting of forest and grassland patches and used clustering techniques and network analyses to identify sets of populations that are more connected to each other than to other sets of populations and estimated the timing of divergence. Our results showed that spatial genetic variation had a significantly modular structure and consisted of four well-defined modules that almost perfectly coincided with habitat features. Genetic divergence was estimated to have occurred about 114 generations ago, coinciding with historic major changes in the landscape. Overall, these results illustrate how populations adapting to different environments become structured genetically within landscapes on small spatial scales.

Highlights

Understanding how the environment shapes species is a central question in evolutionary biology[1,2,3,4]
Identifying the factors that promote genetic differentiation is of interest for understanding the processes initiating the early stages of speciation
We used microsatellite markers to test the hypothesis that differences in phenology, flower morphology and potentially other adaptions to contrasting habitats between grassland and forest populations of the perennial herb P. veris translated into genetic structuring and the occurrence of well-defined genetic entities in the landscape

Summary

Introduction

Understanding how the environment shapes species is a central question in evolutionary biology[1,2,3,4]. When species are distributed across large areas, geographical isolation can limit gene flow and cause strong genetic differentiation, leading to ecotype and even species formation This process can take place either along an ecological gradient or across isolated, well-defined habitat entities[1, 5, 6]. Several reproductive barriers that prevent gene flow can arise when a species occupies contrasting environments within the same geographical region, which in turn can elicit genetic structuring[15, 16] Prezygotic barriers such as differences in flowering time significantly reduce gene transfer between neighboring populations growing under contrasting environmental conditions or in different habitats[17,18,19,20,21]. We hypothesized that restricted gene flow between forest and grassland populations has created genetically structured groups within a mosaic landscape consisting of both grassland and forest habitats and may present the very first signs of ecological speciation

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