Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization

L. Lacey Knowles,Joaquín Ortego

doi:10.1111/mec.16225

Abstract

Alpine biotas are paradigmatic of the countervailing roles of geographical isolation and dispersal during diversification. In temperate regions, repeated distributional shifts driven by Pleistocene climatic oscillations produced both recurrent pulses of population fragmentation and opportunities for gene flow during range expansions. Here, we test whether a model of divergence in isolation vs. with gene flow is more likely in the diversification of flightless alpine grasshoppers of the genus Podisma from the Iberian Peninsula. The answer to this question can also provide key insights about the pace of evolution. Specifically, if the data fit a divergence in isolation model, this suggests rapid evolution of reproductive isolation. Genomic data confirm a Pleistocene origin of the species complex, and multiple analytical approaches revealed limited asymmetric historical hybridization between two taxa. Genomic-based demographic reconstructions, spatial patterns of genetic structure and range shifts inferred from palaeodistribution modelling suggest severe range contraction accompanied by declines in effective population sizes during interglacials (i.e., contemporary populations confined to sky islands are relicts) and expansions during the coldest stages of the Pleistocene in each taxon. Although limited hybridization during secondary contact leads to phylogenetic uncertainty if gene flow is not accommodated when estimating evolutionary relationships, all species exhibit strong genetic cohesiveness. Our study lends support to the notion that the accumulation of incipient differences during periods of isolation were sufficient to lead to lineage persistence, but also that the demographic changes, dispersal constraints and spatial distribution of the sky islands themselves mediated species diversification in temperate alpine biotas.

Highlights

The opportunities for divergence in isolation, and the counteracting effects of gene flow during periods of secondary contact, are quintessential processes of Pleistocene speciation in alpine and montane biotas from temperate regions (Hewitt, 2000)
Our integrative analyses have provided limited evidence of interspecific gene flow during prolonged periods of projected extensive secondary contact and emphasize the genetic cohesiveness of all species within the alpine Podisma complex. These findings support the notion that the interplay among Pleistocene-driven isolation, landscape composition, and species’ traits can trigger the necessary mechanisms for long-lasting genomic diversification and speciation in alpine and montane biotas (Dynesius & Jansson, 2014; Knowles, 2001)
Our comprehensive suite of distributional, demographic and phylogenomic analyses provide a mechanistic explanation for the uncertain phylogenetic relationships among the studied grasshopper species and collectively highlight the important role of Quaternary climatic oscillations in promoting diversification and genetic fragmentation of relictual alpine organisms from temperate regions that currently persist as highly isolated populations in disparate mountain ranges

Summary

| INTRODUCTION

The opportunities for divergence in isolation, and the counteracting effects of gene flow during periods of secondary contact, are quintessential processes of Pleistocene speciation in alpine and montane biotas from temperate regions (Hewitt, 2000). Identifying the causes of phylogenetic conflict (i.e., reticulation vs ILS) is essential for distinguishing among alternative evolutionary pathways (e.g., de Manuel et al, 2016; Schrago & Seuanez, 2019; Thom et al, 2018), which can provide key insights about the pace of speciation (Rosindell et al, 2010; Sukumaran & Knowles, 2017) This task is more daunting in recent Pleistocene radiations in which species may have weak reproductive barriers and short interspeciation times that often co-occur with secondary introgression (i.e., post-d ivergence gene flow) (Nevado et al, 2018; Wen et al, 2016). To accommodate an evolutionary history that may depart from assumptions of divergence in isolation and to gain insights into the processes underlying speciation that includes the possibility of post-divergence gene flow, we integrate a comprehensive suite of phylogenomic and population genomic approaches with palaeoclimate-based reconstructions of species distributions. Using environmental niche modelling and palaeoclimate-based reconstructions of species distributions, we infer range shifts during glacial/interglacial periods in each species and use this framework to determine which expectations in terms of population fragmentation and secondary contact are most probable given species divergence, past demography and introgressive hybridization estimated based on the genomic data

| MATERIALS AND METHODS

| RESULTS

Findings

| DISCUSSION

| CONCLUSIONS