Evidence for adaptive introgression of exons across a hybrid swarm in deer

Abstract

BackgroundSecondary contact between closely related lineages can result in a variety of outcomes, including hybridization, depending upon the strength of reproductive barriers. By examining the extent to which different parts of the genome introgress, it is possible to infer the strength of selection and gain insight into the evolutionary trajectory of lineages. Following secondary contact approximately 8000 years ago in the Pacific Northwest, mule deer (Odocoileus hemionus hemionus) and black-tailed deer (O. h. columbianus) formed a hybrid swarm along the Cascade mountain range despite substantial differences in body size (up to two times) and habitat preference. In this study, we examined genetic population structure, extent of introgression, and selection pressures in freely interbreeding populations of mule deer and black-tailed deer using mitochondrial DNA sequences, 9 microsatellite loci, and 95 SNPs from protein-coding genes.ResultsWe observed bi-directional hybridization and classified approximately one third of the 172 individuals as hybrids, almost all of which were beyond the F1 generation. High genetic differentiation between black-tailed deer and mule deer at protein-coding genes suggests that there is positive divergent selection, though selection on these loci is relatively weak. Contrary to predictions, there was not greater selection on protein-coding genes thought to be associated with immune function and mate choice. Geographic cline analyses were consistent across genetic markers, suggesting long-term stability (over hundreds of generations), and indicated that the center of the hybrid swarm is 20-30 km to the east of the Cascades ridgeline, where there is a steep ecological transition from wet, forested habitat to dry, scrub habitat.ConclusionsOur data are consistent with a genetic boundary between mule deer and black-tailed deer that is porous but maintained by many loci under weak selection having a substantial cumulative effect. The absence of clear reproductive barriers and the consistent centering of geographic clines at a sharp ecotone suggests that ecology is a driver of hybrid swarm dynamics. Adaptive introgression in this study (and others) promotes gene flow and provides valuable insight into selection strength on specific genes and the evolutionary trajectory of hybridizing taxa.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1497-x) contains supplementary material, which is available to authorized users.

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

“…In contrast, a study of recent sole (Solea aegyptiaca x S. senegalensis) hybridization found 52% of all loci exhibited an extreme β value, with 26% of all loci exhibiting a negative β estimate (Souissi et al 2018). For an example of research on an older hybrid zone, blacktailed deer and mule deer have been hybridizing for approximately 8000 years, and when genomic clines were estimated using 95 SNPs, four were found to have extreme β estimates (two positive and two negative; Haines et al 2019). Overall, comparison of genomic cline estimates across studies and taxa is difficult, particularly given the expectation for extreme β values due to drift (Baird, Barton, and Etheridge 2003), the potential for extremely different results depending on the marker panel used (Table 1), the age of a hybrid zone, and rate of admixture between species (Figure 4).…”

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

“…In contrast, a study of recent sole (Solea aegyptiaca x S. senegalensis) hybridization found 52% of all loci exhibited an extreme β value, with 26% of all loci exhibiting a negative β estimate (Souissi et al, 2018). For an example of research on an older hybrid zone, black-tailed deer (Odocoileus hemionus columbianus) and mule deer (O. h. hemionus) have been hybridizing for approximately 8000 years, and when genomic clines were estimated using 95 SNPs, four were found to have extreme β estimates (two positive and two negative; Haines et al, 2019). Overall, comparison of genomic cline estimates across studies and taxa is difficult, particularly given the expectation for extreme β values due to drift (Baird et al, 2003), the potential for extremely different results depending on the marker panel used (Table 1), the age of a hybrid zone, and rate of admixture between species (Figure 3).…”

“…h . hemionus ) have been hybridizing for approximately 8000 years, and when genomic clines were estimated using 95 SNPs, four were found to have extreme β estimates (two positive and two negative; Haines et al, 2019). Overall, comparison of genomic cline estimates across studies and taxa is difficult, particularly given the expectation for extreme β values due to drift (Baird et al, 2003), the potential for extremely different results depending on the marker panel used (Table 1), the age of a hybrid zone, and rate of admixture between species (Figure 3).…”

A Study of Hybridization Between Marmota baibacina and M. sibirica in Their Secondary Contact Zone in Mongolian Altai

“…This may be due to the greater divergence of Nearctic species and, consequently, forming more effective interspecific barriers compared with Palearctic species (Herron et al, 2004;Brandler et al, 2010a). However, neither our study nor those addressing ground squirrel hybrid zones have identified adaptive effects of gene introgression as found in other mammalian hybrid zones [e.g., formation of a hybrid swarm in Odocoileus (Haines et al, 2019); introgressive replacement of the mitochondrial genome in Lepus (Marques et al, 2017)].…”