Range expansion underlies historical introgressive hybridization in the Iberian hare

Abstract

Introgressive hybridization is an important and widespread evolutionary process, but the relative roles of neutral demography and natural selection in promoting massive introgression are difficult to assess and an important matter of debate. Hares from the Iberian Peninsula provide an appropriate system to study this question. In its northern range, the Iberian hare, Lepus granatensis, shows a northwards gradient of increasing mitochondrial DNA (mtDNA) introgression from the arctic/boreal L. timidus, which it presumably replaced after the last glacial maximum. Here, we asked whether a south-north expansion wave of L. granatensis into L. timidus territory could underlie mtDNA introgression, and whether nuclear genes interacting with mitochondria (“mitonuc” genes) were affected. We extended previous RNA-sequencing and produced a comprehensive annotated transcriptome assembly for L. granatensis. We then genotyped 100 discovered nuclear SNPs in 317 specimens spanning the species range. The distribution of allele frequencies across populations suggests a northwards range expansion, particularly in the region of mtDNA introgression. We found no correlation between variants at 39 mitonuc genes and mtDNA introgression frequency. Whether the nuclear and mitochondrial genomes coevolved will need a thorough investigation of the hundreds of mitonuc genes, but range expansion and species replacement likely promoted massive mtDNA introgression.

Complex hybridization patterns in European pond turtles (Emys orbicularis) in the Pyrenean Region

“…Hybridization between closely related taxa is widespread and plays an important evolutionary role because introgression may lead to genetic enrichment 1 , 2 . Introgression is defined as the introduction of foreign genetic material into the genome 1 , which happens in geographic regions where genetically distinct populations meet, mate and hybridize 3 .…”

Genome-wide markers reveal a complex evolutionary history involving divergence and introgression in the Abert’s squirrel (Sciurus aberti) species group

“…A pattern of nuclear introgression without evidence for mitochondrial introgression is somewhat atypical, as mitochondrial DNA is generally assumed to introgress more easily than nuclear DNA [ 3 , 10 , 11 ]. However, nuclear introgression is more difficult to detect with only a handful of genetic markers [ 30 , 31 ], so this assumption may be challenged as more genome-wide datasets are generated in the future. Given that nuclear introgression has potentially important consequences for adaptation and speciation [ 3 – 6 ], future work aimed at identifying genomic regions that have introgressed between Abert’s squirrel populations is necessary to elucidate the relative roles of selective and neutral evolutionary forces in driving the patterns we observed.…”

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

“…Interestingly, all five analysed ancient samples possess the mtDNA haplotype from L. timidus (Table ; Figure S1 in Appendix S1). This mtDNA type is the most frequent in the northern range of L. granatensis , which results from ancient introgression (Melo‐Ferreira et al., , ), during the range replacement of L. timidus in northern Iberia (Acevedo et al., ; Marques et al., ; Seixas et al., ). Our results thus suggest that the post‐glacial northwards expansion of L. granatensis extended beyond the species’ current range, through the Pyrenees, and reached southern France 6 kyr bp .…”

“…These historical hybridization events also affected the nuclear genome, as introgression of nuclear DNA was generally found at low frequencies but widespread, though more frequent in northern Iberia (Melo‐Ferreira et al., ; Seixas, Boursot, & Melo‐Ferreira, ). Patterns of ancient introgression into L. granatensis are compatible with a northwards post‐glacial expansion of the species from southwest Iberia (Marques et al., ) and replacement of historical local populations of L. timidus in the North with repeated hybridization in the invasion front (Melo‐Ferreira, Alves, Rocha, Ferrand, & Boursot, ; Melo‐Ferreira et al., , ; Seixas et al., ). During the post‐glacial westwards invasion of L. europaeus (Forest & Cheylan, ; Lopez‐Martinez, ; Pierpaoli, Riga, Trocchi, & Randi, ; Stamatis et al., ), the species could have then replaced L. timidus and/or L. granatensis populations, though indirect inferences from mtDNA introgression patterns favour a direct contact with L. granatensis in the invasion of northern Iberia (see Melo‐Ferreira et al., ).…”