Locus-specific introgression in young hybrid swarms: drift dominates selection

Abstract

Closely related species that have previously inhabited geographically separated ranges are hybridizing at an increasing rate due to human disruptions. These anthropogenic hybrid zones can be used to study reproductive isolation between species at secondary contact, including examining locus-specific rates of introgression. Introgression is expected to be heterogenous across the genome, reflecting variation in selection. Those loci that introgress especially slowly are good candidates for being involved in reproductive isolation, while those loci that introgress quickly may be involved in adaptive introgression. In the context of conservation, policy makers are especially concerned about introduced alleles moving quickly into the background of a native or endemic species, as these alleles could replace the native alleles in the population, leading to extinction via hybridization. We applied genomic cline analyses to 44997 SNPs to identify loci introgressing at excessive rates when compared to the genome wide expectation in an anthropogenic hybridizing population of red deer and sika in Kintyre Scotland. We found 11.4% of SNPs had cline centers that were significantly different from the genome wide expectation, and 17.6% had excessive rates of introgression. Based on simulations, we believe that many of these markers have diverged from average due to drift, rather than because of selection. Future work could determine the policy implications of allelic-replacement due to drift rather than selection, and could use replicate, geographically distinct hybrid zones to narrow down those loci that are indeed responding to selection in anthropogenic hybrid zones.

Locus‐specific introgression in young hybrid swarms: Drift may dominate selection

“…Physically smaller sika were introduced to Scotland in the late 19 th century, and have since hybridized with the red deer (Ratcliffe, 1987). In some parts of the Kintyre peninsula, Argyll, more than 40% of sampled phenotypic red deer and sika individuals are hybrids according to 50,000 SNP markers, with the majority being the result of multiple generations of backcrossing (McFarlane, Hunter, et al, 2020; McFarlane et al, 2020). Hybrid deer tend towards an intermediate phenotype and thus are smaller, have smaller antlers, and are more likely to have the spots typical of sika than parental species red deer (Bartos et al, 1981).…”

“…Initial hybridization may be constrained by the substantial size difference between species, but it is clear that at least some F1s and many backcrosses are fertile (Harrington, 1979; McFarlane, Hunter, et al, 2020; McFarlane, Senn, et al, 2020). While there is a trend from red deer in the north to sika in the south of Kintyre, the distribution of hybrids does not follow a cline, being instead concentrated in specific areas (Senn et al, 2010), and we have thus recently redefined this system as a “bivariate hybrid zone” (McFarlane, Hunter, et al, 2020; McFarlane & Pemberton, 2019; McFarlane, Senn, et al, 2020). Additionally, in a study using 20 microsatellite markers, there was no evidence that the number of hybrid individuals was changing over a period of 15 years (Senn et al, 2010).…”

“…We used 45K SNP genotypes in 222 Kintyre hybrid deer to estimate genomic clines and show that, as in the other studies cited above, many loci exceed background expectation in terms of direction of introgression α and cline width β . We paid particular attention to the X chromosome, as we have previously found relatively more diagnostic and ancestry informative markers on the X than on the autosomes (McFarlane, Hunter, et al, 2020; McFarlane, Senn, et al, 2020). We then conduct population genetic simulations to investigate admixture scenarios that shed light on the likely roles of drift and selection in generating these results.…”

Admixture mapping reveals loci for carcass mass in red deer x sika hybrids in Kintyre, Scotland

“…It would be interesting to quantify selection on the specific SNPs that we have found here, to determine the potential for these genomic regions to respond to selection on body size. We have previously identified SNPs that are introgressing faster than expected from red deer into sika in our sample (McFarlane et al 2021), but none of the SNPs associated with carcass mass are introgressing faster than the genome-wide expectation, although this doesn't eliminate the possibility of selection for carcass mass alleles within each population. Ideally, we would measure selection on the phenotypes of hybrid individuals with a variety of genotypes to make firm statements about selection on the carcass mass loci we have identified here, and then to make predictions about the potential for adaptive introgression (Taylor and Larson 2019).…”

Niche shifts lead to hybridization between two Amazona parrot sister-species introduced to Southern California

“…This is an appealing hypothesis here, given the selection pressures Southern California parrots are likely experiencing as they adapt to a new niche. However, deviations from neutral diffusion can also be driven by genetic drift (McFarlane et al, 2020), which, given the small population sizes of these species, is likely to be a strong force acting on their genomes. In the future, we plan to sequence more individuals with greater genomic coverage in order to better understand how and why some alleles appear to move between species boundaries whereas others do not.…”