The effect of phylogeographic history on species boundaries: a comparative framework in Hyla tree frogs

Christophe Dufresnes,Nicolas Perrin,Spartak N Litvinchuk,Matthieu Berroneau,Sylvain Dubey

doi:10.1038/s41598-020-62382-4

Christophe Dufresnes, Nicolas Perrin + Show 3 more

Open Access

https://doi.org/10.1038/s41598-020-62382-4

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Abstract

Because it is indicative of reproductive isolation, the amount of genetic introgression across secondary contact zones is increasingly considered in species delimitation. However, patterns of admixture at range margins can be skewed by the regional dynamics of hybrid zones. In this context, we posit an important role for phylogeographic history: hybrid zones located within glacial refugia (putatively formed during the Late-Pleistocene) should be better defined than those located in post-glacial or introduced ranges (putatively formed during the Holocene and the Anthropocene). We test this hypothesis in a speciation continuum of tree frogs from the Western Palearctic (Hyla), featuring ten identified contacts between species spanning Plio-Pleistocene to Miocene divergences. We review the rich phylogeographic literature of this group and examine the overlooked transition between H. arborea and H. molleri in Western France using a multilocus dataset. Our comparative analysis supports a trend that contacts zones resulting from post-glacial expansions and human translocations feature more extensive introgression than those established within refugial areas. Integrating the biogeographic history of incipient species, i.e. their age since first contact together with their genetic divergence, thus appears timely to draw sound evolutionary and taxonomic inferences from patterns of introgression across hybrid zones.

Highlights

Because it is indicative of reproductive isolation, the amount of genetic introgression across secondary contact zones is increasingly considered in species delimitation
Did the biogeographic history of secondary contacts significantly affect their amount of admixture, in turn blurring species delimitation assessments? This question is fundamental for both speciation and systematic biology, but because the answer requires replicate transitions between the same species pairs, or at least between pairs of similar divergence, it has never been formally tested
Based on the distribution of genetic diversity and ecological niche modelling, these studies inferred the location of glacial refugia and routes of post-glacial recolonization for each species, providing insights on the relative age of contact zones that we summarized in File S2

Summary

Introduction

Because it is indicative of reproductive isolation, the amount of genetic introgression across secondary contact zones is increasingly considered in species delimitation. Post-glacial expansions should lead to wide, mosaic parapatric distributions as species colonized new, empty ranges, across the climatically instable northern regions, giving rise to multiple local contacts that may not have reached their ecological or genetic equilibrium yet (e.g.12) As a result, these transitions would exhibit admixture over large distances, even if the interacting species are partially reproductively isolated. Species could start establishing pre-mating barriers earlier in refugial than in post-glacial ranges, where they are expected to experience less gene flow Given these contrasting outcomes, did the biogeographic history of secondary contacts significantly affect their amount of admixture, in turn blurring species delimitation assessments? These scattered observations match our expectations of wider hybrid zones in recently colonized ranges, for the same species pair

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