A genomic footprint of hybrid zone movement in crested newts.

Ben Wielstra,Roger K Butlin,Terry Burke,Jan W Arntzen,Nazan Üzüm,Kurtuluş Olgun,Emin Bozkurt,Aziz Avcı

doi:10.1002/evl3.9

Abstract

Speciation typically involves a stage in which species can still exchange genetic material. Interspecific gene flow is facilitated by the hybrid zones that such species establish upon secondary contact. If one member of a hybridizing species pair displaces the other, their hybrid zone would move across the landscape. Although theory predicts that moving hybrid zones quickly stagnate, hybrid zones tracked over one or a few decades do not always follow such a limitation. This suggests that hybrid zones have the potential to traverse considerable distances over extended periods of time. When hybrid zones move, introgression is predicted to result in biased gene flow of selectively neutral alleles, from the receding species into the advancing species. We test for such a genomic footprint of hybrid zone movement in a pair of crested newt species (genus Triturus) for which we have a priori support for westward hybrid zone movement. We perform a multilocus phylogeographical survey and conduct Bayesian clustering analysis, estimation of ancestry and heterozygosity, and geographical cline analysis. In a 600 km wide area east of the present day hybrid zone a genomic footprint constitutes empirical evidence consistent with westward hybrid zone movement. The crested newt case suggests that hybrid zone movement can occur over an extensive span of time and space. Inferring hybrid zone movement provides fundamental insight into historical biogeography and the speciation process, and we anticipate that hybrid zones will prove to be far more mobile than currently appreciated.

Highlights

A hybrid zone established upon secondary contact may not be at an equilibrium position, based on the competitive abilities of the species involved, or that equilibrium position may shift in response to climate change
The introgression of multiple distinct and geographically structured western mtDNA clades into the eastern species (Fig. 2) supports the hybrid zone movement hypothesis; under positive selection introgressed haplotypes are expected to be identical or similar to haplotypes found in the hybrid zone today
We have tested the hypothesis that a crested newt hybrid zone moved over a considerable time and distance, by documenting unidirectional interspecific introgression for multiple genes

Summary

Introduction

Speciation typically involves the gradual build-up of genetic incompatibility between diverging gene pools (Wu and Ting 2004).The corollary is a stage during the speciation process where reproductive isolation is sufficient for species to maintain their overall integrity while they are still capable of producing hybrids with nonzero fitness, providing a window of opportunity for alleles to be exchanged between species (Mallet 2005; Abbott et al 2013).Hybrid zones, where species meet and admix in nature, are key to understanding introgression (Barton and Hewitt 1985; Hewitt1988); steep clines for those alleles that underperform in the foreign species align with (and in effect define) the species boundary (Barton 2001), while positively selected alleles can permeate the foreign species’ range (Barton 2001; Arnold and Martin 2009), as can neutral ones, albeit with some delay due to the barrier effect of the zone (Barton and Hewitt 1985; Currat et al 2008).Hybrid zones are often positioned at an environmental transition (Endler 1977), suggesting that the species involved are adapted to different environments. A hybrid zone established upon secondary contact may not be at an equilibrium position, based on the competitive abilities of the species involved, or that equilibrium position may shift in response to climate change. Under such circumstances, exogenous selection is expected to promote the replacement of one species by the other (Arntzen 1978; Taylor et al 2015). Exogenous selection is expected to promote the replacement of one species by the other (Arntzen 1978; Taylor et al 2015) This is equivalent to an asymmetry in fitness at many loci across the genome, with hybrid zone movement as a consequence. Such movement has occasionally been observed for hybrid zones tracked over one or a few decades (Arntzen and Wallis 1991; Buggs 2007; Taylor et al 2014; Leaché et al 2017)

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