Genomic heterogeneity of historical gene flow between two species of newts inferred from transcriptome data.

Wiesław Babik,Michał T. Stuglik

doi:10.1002/ece3.2152

Abstract

The role of gene flow in species formation is a major unresolved issue in speciation biology. Progress in this area requires information on the long‐term patterns of gene flow between diverging species. Here, we used thousands of single‐nucleotide polymorphisms derived from transcriptome resequencing and a method modeling the joint frequency spectrum of these polymorphisms to reconstruct patterns of historical gene flow between two Lissotriton newts: L. vulgaris (Lv) and L. montandoni (Lm). We tested several models of divergence including complete isolation and various scenarios of historical gene flow. The model of secondary contact received the highest support. According to this model, the species split from their common ancestor ca. 5.5 million years (MY) ago, evolved in isolation for ca. 2 MY, and have been exchanging genes for the last 3.5 MY Demographic changes have been inferred in both species, with the current effective population size of ca. 0.7 million in Lv and 0.2 million in Lm. The postdivergence gene flow resulted in two‐directional introgression which affected the genomes of both species, but was more pronounced from Lv to Lm. Interestingly, we found evidence for genomic heterogeneity of interspecific gene flow. This study demonstrates the complexity of long‐term gene flow between distinct but incompletely reproductively isolated taxa which divergence was initiated millions of years ago.

Highlights

Speciation, which can be defined as the origin of reproductive barriers among populations (Coyne and Orr 2004), remains an essential problem in evolutionary biology ever since Darwin’s time
We present an overview of the patterns of variation and differentiation based on the Var dataset comprising 954 kb of synonymous sites located in 3832 putative protein coding transcriptome-based gene models (TGMs) (: genes) of six L. montandoni (Lm) and six L. vulgaris (Lv) individuals (Figs. 2 and 3; Table 1)
Of 73,786 synonymous biallelic single-nucleotide polymorphisms (SNP), only 2% represented differences fixed between species, while shared polymorphisms constituted 20.7%, and those private to Lm and Lv 22.7% and 54.7%, respectively (Table 2)

Summary

Introduction

Speciation, which can be defined as the origin of reproductive barriers among populations (Coyne and Orr 2004), remains an essential problem in evolutionary biology ever since Darwin’s time. In a history of divergence, ranges of incipient species often change, and populations may experience periods of allopatry as well as recurrent contact resulting in gene exchange as long as reproductive isolation is not complete (Jiggins and Mallet 2000; Babik et al 2003; Turner et al 2005; Currat et al 2008; Petit and Excoffier 2009; Martin et al 2013; Nadachowska-Brzyska et al 2013; Zielinski et al 2013, 2014) Reconstructing such historical processes – spanning hundreds of thousands or millions of years – constitutes a considerable challenge, complicated by the usual lack of a reliable record of range changes.

Methods

Results

Conclusion