Abstract

AbstractAimCold‐adapted biotas from mid‐latitudes often show small population sizes, harbour low levels of local genetic diversity and are highly vulnerable to extinction due to ongoing climate warming and the progressive shrinking of montane and alpine ecosystems. In this study, we use a suite of analytical approaches to infer the demographic processes that have shaped contemporary patterns of genomic variation in Omocestus bolivari and Omocestus femoralis, two narrow‐endemic and red‐listed Iberian grasshoppers forming highly fragmented populations in the sky island archipelago of the Baetic System.LocationSouth‐eastern Iberia.MethodsWe quantified genomic variation in the two focal taxa and coupled ecological niche models and a spatiotemporally explicit simulation approach based on coalescent theory to determine the relative statistical support of a suite of competing demographic scenarios representing contemporary population isolation (i.e. a predominant role of genetic drift) versus historical connectivity and post‐glacial colonization of sky islands (i.e. pulses of gene flow and genetic drift linked to Pleistocene glacial cycles).ResultsInference of spatial patterns of genetic structure, environmental niche modelling and statistical evaluation of alternative species‐specific demographic models within an approximate Bayesian computation framework collectively supported genetic admixture during glacial periods and post‐glacial colonization of sky islands, rather than long‐term population isolation, as the scenario best explaining the current distribution of genomic variation in the two focal taxa. Moreover, our analyses revealed that isolation in sky islands has also led to extraordinary genetic fragmentation and contributed to reduce local levels of genetic diversity.Main conclusionsThis study exemplifies the potential of integrating genomic and environmental niche modelling data across biological and spatial replicates to determine whether organisms with similar habitat requirements have experienced concerted/idiosyncratic responses to Quaternary climatic oscillations, which can ultimately help to reach more general conclusions about the vulnerability of mountain biodiversity hotspots to ongoing climate warming.

Highlights

  • Distributional shifts in response to Quaternary climatic oscillations had a dramatic impact on biogeographical patterns of species diversity, abundance and local endemism (Hewitt, 1996; Sandel et al, 2011)

  • Our analyses indicate that post-­glacial fragmentation and genetic drift have not blurred the genomic signatures left by historical patterns of population connectivity, the lower levels of genetic diversity in peripheral populations confined to small patches of suitable habitat evidence the genetic consequences of long-­term isolation

  • It must be considered that, according to our own field observations, small habitat patches can often sustain high local densities of the species. This might contribute to maintain large effective population sizes and avoid strong genetic drift even in populations currently confined to tiny sky islands. These results indicate that the genetic makeup of contemporary populations has been shaped in a great extent by historical processes of genetic admixture and drift during the retreat to interglacial refugia (e.g. Knowles & Massatti, 2017), contemporary isolation has contributed to erode the levels of genetic diversity of populations persisting in peripheral sky islands of small size

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Summary

Introduction

Distributional shifts in response to Quaternary climatic oscillations had a dramatic impact on biogeographical patterns of species diversity, abundance and local endemism (Hewitt, 1996; Sandel et al, 2011). The way organisms respond to climate changes strongly depends on species-­specific niche requirements and life-­history traits, which define favourable/ unfavourable climatic periods (glacials or interglacials; Bennett & Provan, 2008) and their capacity to deal with population fragmentation (e.g. microhabitat preferences, dispersal capacity; Massatti & Knowles, 2016; Papadopoulou & Knowles, 2016). These aspects determined the location and extension of Pleistocene refugia, which have played a predominant role on species’ persistence during unfavourable climatic periods and acted as source populations from which species expanded their ranges at the onset of more favourable conditions (Bennett & Provan, 2008). Temperate species currently inhabiting low-­elevation areas generally restricted their distributions to southern refugia during glacial phases (i.e. glacial refugia) and expanded during interglacial periods whereas cold-­adapted species, nowadays presenting fragmented populations at high elevations/latitudes (i.e. interglacial refugia), had much more widespread distributions in glacial stages (Hewitt, 2000)

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