How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels.

Alexis Simon,Christelle Fraïsse,John J Welch,Nicolas Bierne,Petr Strelkov,Cathy Liautard‐Haag,Tahani El Ayari

doi:10.1111/jeb.13709

Abstract

The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study 'replicated' instances of secondary contact between closely related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry-informative panel of such SNPs. We then compared their frequencies in newly sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi-stable variants (Dobzhansky-Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact.

Highlights

Divergence between species is almost always accompanied by hybridisation during phases of contact (Abbott et al, 2013), and so the study of speciation is intertwined with the study of introgression (Aeschbacher, Selby, Willis, & Coop, 2017; Chaturvedi et al, 2019; Duranton et al, 2018; Gagnaire et al, 2018; Martin, Davey, Salazar, & Jiggins, 2019; Roesti, Moser, & Berner, 2013; Schumer et al, 2018)
Our markers were taken from a previous genotypes by sequencing (GBS) study (Fraïsse, Belkhir, et al, 2016), and so we first tested if the markers were still informative in our broader sample
We considered three types of populations: (i) “central” populations, from the centre of the hybrid zone where two species or lineages coexist; (ii) local parental populations (P1 and parent 2 (P2) local) on each side of the hybrid zone and impacted by recent hybridisation; and (iii) distant parental populations (P1 and P2 distant) which are not in direct contact with the focal hybrid zone and so potentially less affected by local introgression

Summary

Introduction

Divergence between species is almost always accompanied by hybridisation during phases of contact (Abbott et al, 2013), and so the study of speciation is intertwined with the study of introgression (Aeschbacher, Selby, Willis, & Coop, 2017; Chaturvedi et al, 2019; Duranton et al, 2018; Gagnaire et al, 2018; Martin, Davey, Salazar, & Jiggins, 2019; Roesti, Moser, & Berner, 2013; Schumer et al, 2018). If some variation is bi-stable (Barton & Turelli, 2011) such that one parental genotype is fitter, but heterozygous or recombinant genotypes are unfit, the spread of the fittest genotype is hindered at the barrier, and thereby contributes to the barrier (Barton, 1979a; Barton & Bengtsson, 1986; Piálek & Barton, 1997). Stochastic processes, such as random drift or variable migration rates, can free the spreading wave of these variants one by one (Piálek & Barton, 1997). The process can be very slow, and so difficult to observe in action

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