Interspecific X-Chromosome and Mitochondrial Dna Introgression in the Iberian Hare: Selection or Allele Surfing?

Abstract

Introgression from a resident species into an invading one is predicted to occur through the demographic process of "allele surfing," and to particularly affect genomic regions transmitted by the lower migrating sex, such as mtDNA. This could explain that northern Iberian populations of Lepus granatensis harbor high frequencies of mtDNA from L. timidus, an arctic hare it replaced there after deglaciation. We report that variation of introgressed timidus-like mtDNA reflects several predicted effects of this process: increasing frequency and diversity in the direction of expansion, strong perpendicular phylogeographic structure and signs of postglacial demographic growth. However, demographic inferences for the granatensis and timidus-like mtDNA lineages suggest the latter may have outcompeted the former in northern Iberia. Autosomal introgression occurs at low frequencies and species-wide rather than only in the north. If this difference with mtDNA resulted from sex-biased migration, an intermediate pattern should prevail for the X-chromosome, but we report species-wide and high-frequency introgression of an X-fragment.Either selection favored this ubiquitous X-introgression, or more complex postglacial expansion patterns prevailed, with different consequences depending on the genomic and geographic region. This illustrates the difficulty of distinguishing demographic and selective effects and the need for genome and species-wide based demographic models.

Home-loving boreal hare mitochondria survived several invasions in Iberia: the relative roles of recurrent hybridisation and allele surfing

“…This would fit the idea that L. granatensis replaced L. timidus in the Northern half of Iberia, favoured by climate warming after the last glacial maximum (Melo-Ferreira et al, 2007). There is evidence of a strong East-West partition of three introgressed mtDNA sublineages, which indicates that the phenomenon occurred at least three times independently during this process (Melo-Ferreira et al, 2011). Therefore, hybridisation was frequent enough for introgression to happen systematically in different parts of the invasion range (although it cannot be completely excluded that selection had a role; see Melo-Ferreira et al, 2011 for discussion).…”

“…For one of these phylogeographic groups of introgressed timidus mtDNA there is also evidence of increased nucleotide diversity towards the north (in the direction of the presumed invasion; Melo-Ferreira et al, 2007). While this pattern would fit the idea of repeated introgression along the invasion front, it was not possible to formally exclude that it results from surfing of de novo mutations (Melo-Ferreira et al, 2011).…”

“…Sequencing of loci located on the X chromosome was either an important extension of previous work (in the cases of Phka2 and Msn; Melo-Ferreira et al, 2009, 2011 or performed de novo (in the case of Smcx and Hprt1) (see Supplementary Tables S2 and S3). These genes were chosen based on their positions along the X chromosome (determined in the European rabbit and assuming synteny with hares, which is vastly observed for the autosomes) : Phka2 and Hprt1 lie close to the telomeres, where recombination is expected to be high, and Smcx and Msn close to the centromere where recombination is expected to be low.…”

“…In theory, rare hybridisation events could suffice for the process to occasionally occur, if drift was important enough at the early stages of invasion and consecutive geographic and demographic expansions rapid enough. However, in some instances such as for the three species of hares (genus Lepus) present in Iberia, the phenomenon appears to have occurred repeatedly and independently, in a quasideterministic manner (Melo-Ferreira et al, 2005, 2007, 2011, 2012. Such a pattern would be best accounted for either if it was driven by selection or if hybridisation occurred repeatedly along the front of advance of the invading species in all cases.…”

“…In addition, the admixture model implemented in Table 1 Number of specimens analysed for the studied molecular markers and absolute frequencies of the mtDNA (cytochrome b) and Y-chromosome (Sry) lineages identified in the L. granatensis and L. europaeus specimens from Á lava, Spain Tables S2 and S3 for a detailed description of the analysed mtDNA and X-chromosome data. d Sequences of 14 of these specimens were from the study by Melo-Ferreira et al (2011). e Sequences of six of these specimens were from the study by Melo-Ferreira et al (2009).…”