Recent Secondary Contacts, Linked Selection, and Variable Recombination Rates Shape Genomic Diversity in the Model Species Anolis carolinensis.

Yann Bourgeois,Stéphane Boissinot,Joseph D Manthey,Robert P Ruggiero,Takashi Gojobori

doi:10.1093/gbe/evz110

Yann Bourgeois, Stéphane Boissinot + Show 3 more

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https://doi.org/10.1093/gbe/evz110

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Abstract

Gaining a better understanding on how selection and neutral processes affect genomic diversity is essential to gain better insights into the mechanisms driving adaptation and speciation. However, the evolutionary processes affecting variation at a genomic scale have not been investigated in most vertebrate lineages. Here, we present the first population genomics survey using whole genome resequencing in the green anole (Anolis carolinensis). Anoles have been intensively studied to understand mechanisms underlying adaptation and speciation. The green anole in particular is an important model to study genome evolution. We quantified how demography, recombination, and selection have led to the current genetic diversity of the green anole by using whole-genome resequencing of five genetic clusters covering the entire species range. The differentiation of green anole’s populations is consistent with a northward expansion from South Florida followed by genetic isolation and subsequent gene flow among adjacent genetic clusters. Dispersal out-of-Florida was accompanied by a drastic population bottleneck followed by a rapid population expansion. This event was accompanied by male-biased dispersal and/or selective sweeps on the X chromosome. We show that the interaction between linked selection and recombination is the main contributor to the genomic landscape of differentiation in the anole genome.

Highlights

IntroductionNucleotide variation along a DNA sequence results from the interactions between multiple processes that either generate new alleles (e.g., recombination, mutation) or affect the fate of these alleles in populations (e.g., selection, demography, and speciation)
Nucleotide variation along a DNA sequence results from the interactions between multiple processes that either generate new alleles or affect the fate of these alleles in populations
We demonstrate that the combined effects of regional variation in recombination rate, linked selection, and migration are responsible for the heterogeneous genomic landscape of diversity and divergence in the green anole

Summary

Introduction

Nucleotide variation along a DNA sequence results from the interactions between multiple processes that either generate new alleles (e.g., recombination, mutation) or affect the fate of these alleles in populations (e.g., selection, demography, and speciation). With the advent of next-generation sequencing and the continuous development of novel analytical tools, it has become possible to properly quantify the impact of recombination (Booker et al 2017; Kawakami et al 2017), selection (Begun and Aquadro 1992; Barrett et al 2008; Mullen and Hoekstra 2008; Cai et al 2009), and demographic history (Gutenkunst et al 2009; Excoffier et al 2013; Roux et al 2016) on diversity patterns in several vertebrates. Assessing the effects of these mechanisms in a range of organisms is crucial to inform current debates about their relative importance (Bierne et al 2011; Kern and Hahn 2018; Pouyet et al 2018; Jensen et al 2019) with a broader set of empirical data

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