Genomics of divergence along a continuum of parapatric population differentiation.

Philine G D Feulner,Erich Bornberg-Bauer,Irene E Samonte,Monika Stoll,Frédéric J J Chain,Tobias L Lenz,Manfred Milinski,Martin Kalbe,Mahesh Panchal,Thorsten B H Reusch,Yun Huang,Christophe Eizaguirre

doi:10.1371/journal.pgen.1004966

Abstract

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.

Highlights

During ecological speciation, divergence along the genome has been observed to be heterogeneous in numerous taxonomic groups [e.g., [1,2,3,4]]
We presented multiple lines of evidence for the role of adaptation shaping the genomic divergence patterns between lake-river populations of three-spined sticklebacks
Aside from adaptive processes, stochastic variation in coalescent times and variable mutation rates could further contribute to the observed heterogeneity of genomic divergence [35]

Summary

Introduction

Divergence along the genome has been observed to be heterogeneous in numerous taxonomic groups [e.g., [1,2,3,4]]. Genetic drift, population expansion, migration, and other demographic events affect the whole genome, whereas natural selection modified by local environmental differences impact only those regions of the genome that affect the respective phenotypes and fitness It is not known whether or not genomic patterns such as the variation of divergence and recombination along the genome tend to follow a predictable evolutionary trajectory as populations proceed along a speciation continuum [7]. If divergence patterns are driven by locus-specific effects of gene flow and divergent selection, the extent of divergence is expected to be more localized than widespread, in line with the “island view” [6] These regions might hold “speciation genes” maintaining reproductive isolation between species including genes underlying a fitness reduction in hybrids [8]. Disentangling such alternative scenarios is a crucial yet challenging step in understanding the genomics of divergence, especially in parapatry where the current and historic extent of migration and gene flow contribute to the overall genomic patterns

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