Abstract

Inferring the demographic history of species is fundamental for understanding their responses to past climate/landscape alterations and improving our predictions about the future impacts of the different components of ongoing global change. Estimating the time-frame at which population fragmentation took place is also critical to determine whether such process was shaped by ancient events (e.g. past climate/geological changes) or if, conversely, it was driven by recent human activities (e.g. habitat loss). We employed genomic data (ddRAD-Seq) to determine the factors shaping contemporary patterns of genetic variation in the Iberian cross-backed grasshopper Dociostaurus crassiusculus, an endangered species with limited dispersal capacity and narrow habitat requirements. Our analyses indicate the presence of two ancient lineages and three genetic clusters resulted from historical processes of population fragmentation (~18–126 ka) that predate the Anthropocene. Landscape genetic analyses indicate that the limits of major river basins are the main geographical feature explaining large-scale patterns of genomic differentiation, with no apparent effect of human-driven habitat fragmentation. Overall, our study highlights the importance of detailed phylogeographic, demographic and spatially-explicit landscape analyses to identify evolutionary significant units and determine the relative impact of historical vs. anthropogenic factors on processes of genetic fragmentation in taxa of great conservation concern.

Highlights

  • Inferring the evolutionary and demographic history of species and populations is fundamental for understanding how they were impacted by past environmental and landscape alterations and anticipating their responses to different components of global change such as climatic variations[1,2,3], habitat loss[4] or the emergence of infectious diseases[5]

  • Genomic data revealed that populations of the endangered Iberian grasshopper D. crassiusculus show a marked hierarchical genetic structure, with the presence of two highly divergent cryptic lineages (Fig. 3) that comprise three genetic clusters (Figs 1 and 2)

  • The consistent support for models including gene flow between ancestral populations, indicate that vicariance with multiple contacts is likely to have led to the current genetic structure of the species

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Summary

Introduction

Inferring the evolutionary and demographic history of species and populations is fundamental for understanding how they were impacted by past environmental and landscape alterations and anticipating their responses to different components of global change such as climatic variations[1,2,3], habitat loss[4] or the emergence of infectious diseases[5]. Genetic and spatial information has been successfully integrated to infer dispersal routes across different habitat types[20], identify natural barriers to dispersal (e.g. rivers[24], topography[25], geology26) and determine the consequences of human activities on disrupting gene flow of natural populations (e.g. agriculture[27,28], infrastructures[29]) For this reason, testing alternative spatially-explicit scenarios of population connectivity under a landscape genetic framework can help to determine the relative role of human and natural barriers to gene flow on structuring present-day patterns of genetic variation[30]. These narrow habitat requirements, together with the reduced flying capacity of the species and the progressive loss of its natural habitat by human activities, has led that all populations of D. crassiusculus are nowadays extremely fragmented and at high risk of extinction by stochastic phenomena[3,49]

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