Glacial connectivity and current population fragmentation in sky islands explain the contemporary distribution of genomic variation in two narrow-endemic montane grasshoppers from a biodiversity hotspot

RESEARCH ARTICLE

Glacial connectivity and current population fragmentation in sky islands explain the contemporary distribution of genomic variation in two narrow-endemic montane grasshoppers from a biodiversity hotspot.

Abstract

Aim: Cold-adapted biotas from mid-latitudes often show small population sizes, harbor 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.

Location: South-eastern Iberia.

Methods: We 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).

Results: Inference of spatial patterns of genetic structure, environmental niche modeling 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 conclusions: This 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.

One INTRODUCTION |

Distributional shifts in response to Quaternary climatic oscillations had a dramatic impact on biogeographical patterns of species diversity, abundance and local endemism. These cycles, in particular the high-amplitude climatic changes characterizing the mid and late Pleistocene (less than zero point eight million years ago), have also shaped the distribution and spatial patterns of genetic variation in many organisms. However, multiple studies have documented considerable heterogeneity across regions and taxa in the demographic consequences of Pleistocene glacial cycles. On the one hand, the impact of Pleistocene glaciations strongly depended on latitude and regional topography, with extinction-recolonization dynamics at higher latitudes (i.e. "southern richness to northern purity" paradigm) and elevational shifts and more complex processes of population fragmentation and connectivity at lower latitudes such as the tropics or temperate regions (e.g. "refugia within refugia" concept). On the other hand, the way organisms respond to climate changes strongly depends on species-specific niche requirements and life-history traits, which define favorable/unfavorable climatic periods (glacials or interglacials) and their capacity to deal with population fragmentation (e.g. microhabitat preferences, dispersal capacity). These aspects determined the location and extension of Pleistocene refugia, which have played a predominant role on species' persistence during unfavorable climatic periods and acted as source populations from which species expanded their ranges at the onset of more favorable conditions. 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.

Mid- and low-latitude alpine and montane taxa represent small-scale replicates of cold-adapted species living at high latitudes. Sky islands are a paradigmatic example of interglacial refugia in which alpine and montane organisms currently form highly isolated populations in mountain ranges separated from each other by intervening valleys with unsuitable environmental conditions.

Changing climatic conditions causes suitable habitats to expand or shrink along elevational gradients, leading to alternating periods of population isolation and connectivity. Periods of isolation on mountain tops are expected to lead to demographic bottlenecks, genetic drift and divergence among populations, while periods of connectivity allow for dispersal and gene flow among formerly isolated populations. Species restricted to sky islands often show unique patterns of population genetic structure resulting from climate-induced distributional shifts, processes that in some cases have led to lineage diversification and speciation. Therefore, montane habitats are often important hotspots of intraspecific genetic diversity, species richness and local endemism, providing an excellent study system for understanding how climatic changes associated with Pleistocene glacial cycles impacted species distributions, demography and genetic diversification. Their study takes particular relevance if we consider that species restricted to sky islands often show small population sizes, harbor reduced levels of local genetic diversity and are highly vulnerable to extinction due to ongoing climate warming and the progressive shrink of alpine ecosystems.

South-eastern Iberia constitutes an important biodiversity hotspot due to the interplay among a complex geological history, an extraordinarily complex topography and a limited impact of Quaternary glations. The presence of vast areas free of permanent ice during the coldest stages of the Pleistocene made this region an important glacial refugium for warm-temperate taxa. At the same time, the mountain ranges of the region, Baetic system, greater than three thousand meters, constitute important interglacial refugia for several cold-adapted organisms that currently persist in severely fragmented populations at high elevation patches of suitable habitat and contribute disproportionally to the extraordinary rates of local endemism of the area. This offers an ideal biogeographical setting to jointly study the genetic consequences of long-term population fragmentation in this sky island system and assess the time-scale at which past distributional shifts have shaped contemporary patterns of genetic variation in alpine organisms from mid-latitudes.

Here, we use genomic data obtained via restriction site-associated DNA sequencing and a suite of analytical approaches to shed light on the demographic processes underlying contemporary patterns of genetic variation in the grasshoppers Omocestus bolivari Chopard, nineteen thirty-nine, and Omocestus femoralis Bolívar, nineteen oh eight, two narrow-endemic Iberian species inhabiting high elevation areas in the sky island archipelago of the Baetic System. The two taxa are closely related non-sister species that present adjacent but not overlapping distributions, both occupying similar open habitats of thorny shrub formations located at the upper, greater than one thousand five hundred meters, thermoclimatic belts of the Mediterranean region. They are graminivorous, univoltine, i.e. a single generation per year, and present similar phenologies, with adult population peaks in July. The distribution range of the two species includes sky islands of varying size, ranging from large ones in the main massifs of the region, O. bolivari: Sierra Nevada and Sierra de Baza-Filabres; O. femoralis: Sierra de Cazorla, to tiny patches of suitable habitat located in isolated mountains with maximum elevations close to the lower altitudinal limit of the species. By using these two species of uniform ecological and life-history traits as independent replicates, we exemplify how the integration of genomic and environmental niche modelling data within a comparative framework can help to elucidate the responses of species with similar habitat requirements to processes of population fragmentation/connectivity driven by Pleistocene climatic oscillations. This can ultimately help to understand the temporal scale at which such processes have shaped contemporary patterns of genetic variation in the focal species and other co-distributed organisms with analogous environmental niches. In a first step, (a) we tested whether observed patterns of genomic variation in the two biological replicates reflect the signals of historical population connectivity, i.e. gene flow during glacial periods and subsequent colonization and population isolation in sky islands, i.e. genetic drift during interglacial periods, or, rather, if post-glacial population fragmentation and genetic drift after the Pleistocene-Holocene transition have entirely monopolized the genetic makeup of contemporary populations. Specifically, we quantified genetic structure and coupled ecological niche models and a spatio-temporally explicit simulation approach based on coalescent theory to mimic complex demographic processes under a suite of scenarios representing historical gene flow and post-glacial colonization in sky islands versus contemporary population isolation. The expectations under these alternative scenarios were tested and validated against observed genomic data within an approximate Bayesian computation framework. In a second step, (b) we analysed the impact of sky island size and the spatial location of contemporary populations on their demographic fate and levels of genetic variation. To this end, we tested the hypothesis that genetic diversity is positively associated with the geographic centrality of populations and habitat patch size and used demographic reconstructions based on genomic data to determine whether changes in effective population size, N sub E, over time differed between sky islands of contrasting size and degree of peripheral location.