Post‐glacial range revolutions in South European hares (Lepus spp.): Insights from ancient DNA and ecological niche modelling

Abstract

Aim:The distribution of hares (Lepus spp.) in southern Europe was markedly different at the Last Glacial Maximum. Historical hybridization during range replacements led to high frequencies of mtDNA introgression from Lepus timidus into populations of three other species in northern Iberian Peninsula, even though L. timidus subsequently disappeared from the region. We use palaeontological records to provide new insights on the biogeographic history of these range replacements, combining ancient DNA and ecological niche modelling.Location: Southern France. Taxon: Hares (genus Lepus).Methods: DNA was extracted from hare bones collected at Neolithic sites in southern France (5.5-7.5 thousand years before present; kyr BP) with uncertain species assignment. One mtDNA fragment was sequenced and 27 SNPs from 11 nuclear genes with species-diagnostic information were genotyped. Distributions of L. granatensis, L. europaeus, and L. timidus were modelled using spatial and bioclimatic predictors, and the favourability function. Each model was transferred to 6 kyr BP and favourabilities were combined to determine the species with the highest environmental favourability in each sampled locality.Results: Ancient DNA analysis showed that the screened specimens belong to L. granatensis, a species presently confined to the Iberian Peninsula, but carried mtDNA haplotypes from L. timidus. Niche models show that L. granatensis achieved highest favourability in southern France 6 kyr BP reinforcing the molecular evidences.Main conclusions: L. granatensis replaced L. timidus populations from Iberia to southern France, being present in this region 5.5 kyr BP. Subsequent westwards invasion of L. europaeus likely replaced these L. granatensis populations towards northern Iberia, establishing current ranges. Despite successive species replacements, introgressed mtDNA haplotypes from L. timidus mark the distribution of the species in northern Iberian Peninsula before it disappeared in the region. Characterizing complex biogeographic histories of interacting species is a key to understand processes that led to current distributions of genetic diversity.

Historical hybrid zone movement: More pervasive than appreciated

“…Even if sufficient material is available, a condition for employing the fossil/pollen record is that the interacting populations can be distinguished, despite their similarity as implied by hybridization. While one study on birch trees succeeded in identification of hybridizing taxa from pollen alone (Wang et al., ), another one on hares resorted to sequencing ancient DNA to establish to which taxon fossils belonged (Lado et al., ) (Table ). Given these limitations, the fossil/pollen record is unlikely to be broadly applicable to inferring historical hybrid zone movement.Range shifts of hybridizing populations have been inferred from species distribution modelling, as predicted habitat suitability for the population presumed to have been replaced decreased over time, while the reverse applies to the supposedly invading population (Figure ).…”

“…Even if sufficient material is available, a condition for employing the fossil/pollen record is that the interacting populations can be distinguished, despite their similarity as implied by hybridization. While one study on birch trees succeeded in identification of hybridizing taxa from pollen alone (Wang et al, 2014), another one on hares resorted to sequencing ancient DNA to establish to which taxon fossils belonged (Lado et al, 2018) (Table 1).…”

Genetic traces of hybrid zone movement across a fragmented habitat

“…Although hybrid zone movement has not previously been considered to be common (Buggs, 2007), the spatial and genetic signatures of moving hybrid zones are by now been well documented in a wide range of vertebrate taxa including fishes (Souissi et al, 2018), salamanders (Arntzen & Wallis, 1991; Wielstra, Burke, Butlin, Arntzen, et al, 2017), toads (Arntzen, 1978, 2019; Arntzen et al, 2017), birds (Carling & Zuckerberg, 2011) and mammals (Lado et al, 2018; Macholán et al, 2011). Two important reservations apply to our interpretations.…”

Genome admixture among four hare species in Iberia: focus on the broom hare (Lepus castroviejoi)

“…Their present distribution ranges are the result of recurrent range changes, overlaps and hybridization events since late Pleistocene (Alves et al, 2008b;Melo-Ferreira et al, 2012;Seixas et al, 2018). The mountain hare (Lepus timidus) currently ranges from northern Europe to Far East Russia, and is present in some isolated populations, such as in Ireland, Great Britain and the Alps (Angerbjörn, 2018), but palaeontological records show that it was present much further south at the last glacial maximum, reaching the Iberian Peninsula (Altuna, 1970;Lado et al, 2018). Its subsequent northward retreat resulted from the post-glacial climate warming and possibly also from the invasion of temperate species (Melo-Ferreira et al, 2007;Acevedo et al, 2015).…”