An official website of the United States government
Abstract Divergent adaptation can promote ecological speciation if hybrids have reduced fitness because they are poorly adapted to either parental niche. We tested for ecologically dependent, postzygotic isolation between two subspecies of Swainson’s thrushes, which form a migratory divide and hybrid zone in western North America. To do this, we translocated backcrossed and admixed birds from the hybrid zone into the range of each subspecies in the beginning of fall migration. We estimated a proxy for their survival on migration and migratory behaviour using automated radio tracking. Apparent survival of birds in the two environments did not depend on their genomic ancestry, suggesting that Swainson’s thrushes’ divergent adaptation to different fall migration routes does not fit the classic model of ecological speciation. We propose an alternate scenario where ecological selection on migration may interact with intrinsic maladaptation in hybrids to cause hybrid survival on migration. By translocating birds from the same genomic backgrounds into different environments, our experiment also allowed us to distinguish between the effects of environmental relative to genetic contributors to their migratory behaviour. We found evidence that both genetic and environmental factors influence migratory behaviour, as an effect of genomic ancestry on initial migratory trajectories depended on the start location for migration but birds ultimately followed expected routes given their genomic ancestries.
more »
« less
Migratory divides coincide with reproductive barriers across replicated avian hybrid zones above the Tibetan Plateau
Abstract Migratory divides are proposed to be catalysts for speciation across a diversity of taxa. However, it is difficult to test the relative contributions of migratory behaviour vs. other divergent traits to reproductive isolation. Comparing hybrid zones with and without migratory divides offers a rare opportunity to directly examine the contribution of divergent migratory behaviour to reproductive barriers. We show that across replicate sampling transects of two pairs of barn swallow (Hirundo rustica) subspecies, strong reproductive isolation coincided with a migratory divide spanning 20 degrees of latitude. A third subspecies pair exhibited no evidence for a migratory divide and hybridised extensively. Within migratory divides, overwintering habitats were associated with assortative mating, implicating a central contribution of divergent migratory behaviour to reproductive barriers. The remarkable geographic coincidence between migratory divides and genetic breaks supports a long‐standing hypothesis that the Tibetan Plateau is a substantial barrier contributing to the diversity of Siberian avifauna.
more »
« less
- PAR ID:
- 10457088
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 23
- Issue:
- 2
- ISSN:
- 1461-023X
- Format(s):
- Medium: X Size: p. 231-241
- Size(s):
- p. 231-241
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Migratory divides, hybrid zones between populations that use different seasonal migration routes, are hypothesised to contribute to speciation. Specifically, relative to parental species, hybrids at divides are predicted to exhibit (1) intermediate migratory behaviour and (2) reduced fitness as a result. We provide the first direct test of the second prediction here with one of the largest existing avian tracking datasets, leveraging a divide between Swainson's thrushes where the first prediction is supported. Using detection rates as a proxy for survival, our results supported the migratory divide hypothesis with lower survival rates for hybrids than parental forms. This finding was juvenile‐specific (vs. adults), suggesting selection against hybrids is stronger earlier in life. Reduced hybrid survival was not explained by selection against intermediate phenotypes or negative interactions among phenotypes. Additional work connecting specific features of migration is needed, but these patterns provide strong support for migration as an ecological driver of speciation.more » « less
-
ABSTRACT Tree species are often locally adapted to their environments, but the extent to which environmental adaptation contributes to incipient speciation is unclear. One of the rarest pines in the world, Torrey pine (Pinus torreyanaParry), persists naturally across one island and one mainland population in southern California. The two populations are morphologically and genetically differentiated but experience some connectivity, making it an ideal system for assessing the evolution of reproductive isolation. Previous work has found evidence of heterosis in F1 mainland‐island hybrids, suggesting genetic rescue could be beneficial in the absence of reproductive barriers. Using ddRADseq and GWAS for a common garden experiment of island, mainland, and F1 individuals, we identified candidate loci for environmentally driven reproductive isolation, their function, and their relationship to fitness proxies. By simulating neutral evolution and admixture between the two populations, we identified loci that exhibited reduced heterozygosity in the F1s, evidence of selection against admixture. SNPs with reduced F1 heterozygosity were enriched for growth and pollination functions, suggesting genetic variants that could be involved in the evolution of reproductive barriers between populations. One locus with reduced F1 heterozygosity exhibited strong associations with growth and reproductive fitness proxies in the common garden, with the mainland allele conferring increased fitness. If this locus experiences divergent selection in the two natural populations, it could promote their reproductive isolation. Finally, although hybridization largely reduced allele fixation in the F1s initially, indicating heterosis is likely due to the masking of deleterious alleles, the emergence of reproductive isolation between populations may diminish the longer‐term benefits of genetic rescue in F2 or advanced‐generation hybrids. As Torrey pine is a candidate for interpopulation genetic rescue, caution is warranted where longer‐term gene flow between diverged populations may result in reduced fitness if barriers have evolved.more » « less
-
Abstract In high-latitude species with high dispersal ability, such as long-distance migratory birds, populations are often assumed to exhibit little genetic structure due to high gene flow or recent postglacial expansion. We sequenced over 120 low-coverage whole genomes from across the breeding range of a long-distance migratory bird, the Veery (Catharus fuscescens), revealing strong evidence for isolation by distance. Additionally, we found distinct genetic structure between boreal, western montane U.S., and southern Appalachian sampling regions. We suggest that population genetic structure in this highly migratory species is detectable with the high resolution afforded by whole-genomic data because, similar to many migratory birds, the Veery exhibits high breeding-site fidelity, which likely limits gene flow. Resolution of isolation by distance across the breeding range was sufficient to assign likely breeding origins of individuals sampled in this species’ poorly understood South American nonbreeding range, demonstrating the potential to assess migratory connectivity in this species using genomic data. As the Veery’s breeding range extends across both historically glaciated and unglaciated regions in North America, we also evaluated whether contemporary patterns of structure and genetic diversity are consistent with historical population isolation in glacial refugia. We found that patterns of genetic diversity did not support southern montane regions (southern Appalachians or western U.S. mountains) as glacial refugia. Overall, our findings suggest that isolation by distance yields subtle associations between genetic structure and geography across the breeding range of this highly vagile species even in the absence of obvious historical vicariance or contemporary barriers to dispersal.more » « less
-
Abstract Animals generally benefit from their gastrointestinal microbiome, but the factors that influence the composition and dynamics of their microbiota remain poorly understood. Studies of nonmodel host species can illuminate how microbiota and their hosts interact in natural environments. We investigated the role of migratory behaviour in shaping the gut microbiota of free‐ranging barn swallows (Hirundo rustica) by studying co‐occurring migrant and resident subspecies sampled during the autumn migration at a migratory bottleneck. We found that within‐host microbial richness (α‐diversity) was similar between migrant and resident microbial communities. In contrast, we found that microbial communities (β‐diversity) were significantly different between groups regarding both microbes present and their relative abundances. Compositional differences were found for 36 bacterial genera, with 27 exhibiting greater abundance in migrants and nine exhibiting greater abundance in residents. There was heightened abundance ofMycoplasmaspp. andCorynebacteriumspp. in migrants, a pattern shared by other studies of migratory species. Screens for key regional pathogens revealed that neither residents nor migrants carried avian influenza viruses and Newcastle disease virus, suggesting that the status of these diseases did not underlie observed differences in microbiome composition. Furthermore, the prevalence and abundance ofSalmonellaspp., as determined from microbiome data and cultural assays, were both low and similar across the groups. Overall, our results indicate that microbial composition differs between migratory and resident barn swallows, even when they are conspecific and sympatrically occurring. Differences in host origins (breeding sites) may result in microbial community divergence, and varied behaviours throughout the annual cycle (e.g., migration) could further differentiate compositional structure as it relates to functional needs.more » « less
