Abstract

The red deer (Cervus elaphus) is a widespread wild ungulate in Europe that has suffered strong anthropogenic impacts over their distribution during the last centuries, but also at the present time, due its economic importance as a game species. Here we focus on the evolutionary history of the red deer in Iberia, one of the three main southern refugial areas for temperate species in Europe, and addressed the hypothesis of a cryptic refugia at higher latitudes during the Last Glacial Maximum (LGM). A total of 911 individuals were sampled, genotyped for 34 microsatellites specifically developed for red deer and sequenced for a fragment of 670 bp of the mitochondrial (mtDNA) D-loop. The results were combined with published mtDNA sequences, and integrated with species distribution models and historical European paleo-distribution data, in order to further examine the alternative glacial refugial models and the influence of cryptic refugia on European postglacial colonization history. Clear genetic differentiation between Iberian and European contemporary populations was observed at nuclear and mtDNA levels, despite the mtDNA haplotypes central to the phylogenetic network are present across western Europe (including Iberia) suggesting a panmictic population in the past. Species distribution models, fossil records and genetic data support a timing of divergence between Iberian and European populations that overlap with the LGM. A notable population structure was also found within the Iberian Peninsula, although several populations displayed high levels of admixture as a consequence of recent red deer translocations. Five D-loop sub-lineages were found in Iberia that belong to the Western European mtDNA lineage, while there were four main clusters based on analysis of nuclear markers. Regarding glacial refugial models, our findings provide detailed support for the hypothesis that red deer may have persisted in cryptic northern refugia in western Europe during the LGM, most likely in southern France, southern Ireland, or in a region between them (continental shelf), and these regions were the source of individuals during the European re-colonization. This evidence heightens the importance of conserving the high mitochondrial and nuclear diversity currently observed in Iberian populations.

Highlights

  • Understanding demographic and evolutionary history is fundamental to explain current species distributions and to forecast future trends under global climate change [1,2]

  • Clarifying in which regions species persisted during glaciations, as well as the timing and mode of postglacial expansions, is essential to understand evolutionary processes such as adaptation, speciation and extinction [14,111]

  • The divergence of the Western European lineage may be related to a partial discontinuity in red deer habitat suitability evident at 120 ky BP between western and eastern Europe (Fig 8), i.e. during the Eemian interglacial age (127–117 ky BP) [112] and presumably present during the Saalian glacial period [113] that preceded it

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Summary

Introduction

Understanding demographic and evolutionary history is fundamental to explain current species distributions and to forecast future trends under global climate change [1,2]. We extend substantially on those studies, by employing a multidisciplinary approach involving mtDNA and nuclear data, species distribution models and fossil evidence in populations across Europe This approach allows an unprecedented consideration of the LGM refugia of the red deer as well as the role of cryptic refugia in western Europe. Red deer distribution and density reached a minimum during that period, but a demographic expansion has been observed over the last decades, mainly promoted by humans [40,41] Despite these recent anthropogenic impacts, the demographic history of Iberian populations is still marked by past natural biogeographical events [36,42]. We combined nuclear (34 microsatellite loci developed for red deer) and mitochondrial (D-loop sequences) markers, together with species distribution modeling and paleo-distribution data, to elucidate red deer evolutionary history in Iberia and address the hypothesis of a cryptic refugium at higher latitudes in Europe during the LGM

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