Today, published in Molecular Ecology: our paper comparing patterns of genomic differentiation across three hybridizing species pairs of warblers. This paper is the culmination of many years of work by a great group of 10 collaborators.
Irwin, D.E., B. Milá, D.P.L. Toews, A. Brelsford, H.L. Kenyon, A.N. Porter, C. Grossen, K.E. Delmore, M. Alcaide, and J.H. Irwin. 2018. A comparison of genomic islands of differentiation across three young avian species pairs. Molecular Ecology, online Early View: https://doi.org/10.1111/mec.14858
Detailed evaluations of genomic variation between sister species often reveal distinct chromosomal regions of high relative differentiation (i.e., “islands of differentiation” in FST), but there is much debate regarding the causes of this pattern. We briefly review the prominent models of genomic islands of differentiation and compare patterns of genomic differentiation in three closely related pairs of New World warblers with the goal of evaluating support for the four models. Each pair (MacGillivray’s/mourning warblers; Townsend’s/black‐throated green warblers; and Audubon’s/myrtle warblers) consists of forms that were likely separated in western and eastern North American refugia during cycles of Pleistocene glaciations and have now come into contact in western Canada, where each forms a narrow hybrid zone. We show strong differences between pairs in their patterns of genomic heterogeneity in FST, suggesting differing selective forces and/or differing genomic responses to similar selective forces among the three pairs. Across most of the genome, levels of within‐group nucleotide diversity (πWithin) are almost as large as levels of between‐group nucleotide distance (πBetween) within each pair, suggesting recent common ancestry and/or gene flow. In two pairs, a pattern of the FSTpeaks having low πBetween suggests that selective sweeps spread between geographically differentiated groups, followed by local differentiation. This “sweep‐before‐differentiation” model is consistent with signatures of gene flow within the yellow‐rumped warbler species complex. These findings add to our growing understanding of speciation as a complex process that can involve phases of adaptive introgression among partially differentiated populations.
Congrats to Kenneth Askelson for his excellent M.Sc. defence! Kenny’s thesis is titled “Genomic Differentiation of Northern Goshawks in Coastal British Columbia.”
Darren has published a review of sex chromosomes evolution and speciation in birds and other ZW systems. This is an invited submission for a special issue of Molecular Ecology, on “Sex Chromosomes and Speciation.”
Here’s the citation and link:
Irwin, D.E. 2018. Sex chromosomes and speciation in birds and other ZW systems. Molecular Ecology, online Early View: https://doi.org/10.1111/mec.14537
Congrats to Alan Brelsford and David Toews, co-first authors on our new paper on the loci underlying colour pattern differences across the Audubon’s / myrtle warbler hybrid zone.
Brelsford, A.*, D.P.L. Toews*, and D.E. Irwin. 2017. Admixture mapping in a hybrid zone reveals loci associated with avian feather coloration. Proceedings B 284: 20171106. *Shared first authorship. Link
The UBC Science press release: Link
The key figure from the paper, showing the result of a genome-wide association study of colour differences between the two forms:
Identifying the genetic bases for colour patterns has provided important insights into the control and expression of pigmentation and how these characteristics influence fitness. However, much more is known about the genetic bases for traits based on melanin pigments than for traits based on another major class of pigments, carotenoids. Here, we use natural admixture in a hybrid zone between Audubon’s and myrtle warblers (Setophaga coronata auduboni/S. c. coronata) to identify genomic regions associated with both types of pigmentation. Warblers are known for rapid speciation and dramatic differences in plumage. For each of five plumage coloration traits, we found highly significant associations with multiple single-nucleotide polymorphisms (SNPs) across the genome and these were clustered in discrete regions. Regions near significantly associated SNPs were enriched for genes associated with keratin filaments, fibrils that make up feathers. A carotenoid-based trait that differs between the taxa—throat colour—had more than a dozen genomic regions of association. One cluster of SNPs for this trait overlaps the Scavenger Receptor Class F Member 2 (SCARF2) gene. Other scavenger receptors are presumed to be expressed at target tissues and involved in the selective movement of carotenoids into the target cells, making SCARF2 a plausible new candidate for carotenoid processing. In addition, two melanin-based plumage traits—colours of the eye line and eye spot—show very strong associations with a single genomic region mapping to chromosome 20 in the zebra finch. These findings indicate that only a subset of the genomic regions differentiated between these two warblers are associated with the plumage differences between them and demonstrate the utility of reduced-representation genomic scans in hybrid zones.
Congrats to co-authors David Toews and Julian Heavyside on our publication showing that the Myrtle Warblers (a form of Yellow-rumped Warbler) migrating down the Pacific Coast of North America are primarily breeding in Alaska, the Yukon, and northern BC, rather than further east.
The UBC Science press release: Isotope fingerprints in feathers reveal songbirds’ secret breeding grounds
Toews, D.P.L., J. Heavyside, and D.E. Irwin. 2017. Linking the wintering and breeding grounds of warblers along the Pacific Flyway. Ecology and Evolution, online Early View. DOI: 10.1002/ece3.3222 Link (open access!)
Long-distance migration is a behavior that is exhibited by many animal groups. The evolution of novel migration routes can play an important role in range expansions, ecological interactions, and speciation. New migration routes may evolve in response to selection in favor of reducing distance between breeding and wintering areas, or avoiding navigational barriers. Many migratory changes are likely to evolve gradually and are therefore difficult to study. Here, we attempt to connect breeding and wintering populations of myrtle warblers (Setophaga coronata coronata) to better understand the possible evolution of distinct migration routes within this species. Myrtle warblers, unlike most other warblers with breeding ranges primarily in eastern North America, have two disjunct overwintering concentrations—one in the southeastern USA and one along the Pacific Coast—and presumably distinct routes to-and-from these locations. We studied both myrtle and Audubon’s warblers (S. c. auduboni) captured during their spring migration along the Pacific Coast, south of the narrow region where these two taxa hybridize. Using stable hydrogen isotopes and biometric data, we show that those myrtle warblers wintering along the southern Pacific Coast of North America are likely to breed at high latitudes in Alaska and the Yukon rather than in Alberta or further east. Our interpretation is that the evolution of this wintering range and migration route along the Pacific Coast may have facilitated the breeding expansion of myrtle warblers into northwestern North America. Moreover, these data suggest that there may be a migratory divide within genetically similar populations of myrtle warblers.
Myrtle warbler (copyright: Darren Irwin)
Congrats to lead author Ildiko Szabo and coauthors Kimberly Walters and James Rourke on our publication documenting the first specimen of House Swift in the Americas:
Szabo, I., K. Walters, J. Rourke, and D.E. Irwin. 2017. First record of House Swift (Apus nipalensis) in the Americas. Wilson Journal of Ornithology 129: 411-416. Link
A carcass of a House Swift (Apus nipalensis) found in Ladner, British Columbia on 18 May 2012 appears to be the first documented record of this species in the Americas. Identification is based on DNA sequencing and morphometric characters. University of British Columbia Beaty Biodiversity Museum Cowan Tetrapod Collection catalogue number B017056 has been assigned to this specimen (round study skin, spread wing, partial skeleton, and tissue samples).
Feel free to email me for a PDF of the full publication.
Congrats to lead author Haley Kenyon and coauthors Miguel Alcaide and David Toews on our publication comparing song and genetic variation across the Townsend’s / Black-throated Green Warbler hybrid zone. I think this paper makes a particularly interesting contribution by jointly considering cultural evolution, genetic evolution, and hybrid zone theory.
Kenyon, H.L., M. Alcaide, D.P.L. Toews, and D.E. Irwin. Cultural isolation is greater than genetic isolation across an avian hybrid zone. Journal of Evolutionary Biology, online Early View: doi:10.1111/jeb.12989 Link
Elucidating the relationship between genetic and cultural evolution is important in understanding speciation, as learned premating barriers might be involved in maintaining species differences. Here, we test this relationship by examining a widely recognized premating barrier, bird song, in a hybrid zone between black-throated green (Setophaga virens) and Townsend’s warblers (S. townsendi). We use song analysis, genomic techniques and playback experiments to characterize the cultural and genetic backgrounds of individuals in this region, expecting that if song is an important reproductive barrier between these species, there should be a strong relationship between song and genotype. We show that songs in the hybrid zone correspond to the distinctly different songs found in allopatry but that song and genotype are not tightly coupled in sympatry. Allopatric individuals responded only to local songs, indicating that individuals may have learned to respond to songs they commonly hear. We observed discordance between song and genotype clines; a narrower cline suggests that cultural selection on song is stronger than natural selection on genotype. These findings indicate that song is unlikely to play a role in reproductive isolation between these species, and we suggest that spatial variation in song may nonetheless be maintained by frequency-dependent cultural selection. This decoupling of genes and culture may contribute to hybridization in this region.
Feel free to email me for a PDF of the full publication.
Published September 8th in Molecular Ecology:
Irwin, D.E., M. Alcaide, K.E. Delmore, J.H. Irwin, and G.L. Owens. 2016. Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in a ring species. Molecular Ecology, online Early View: doi:10.1111/mec.13792 Link
The Abstract: Recent technological developments allow investigation of the repeatability of evolution at the genomic level. Such investigation is particularly powerful when applied to a ring species, in which spatial variation represents changes during the evolution of two species from one. We examined genomic variation among three subspecies of the greenish warbler ring species, using genotypes at 13 013 950 nucleotide sites along a new greenish warbler consensus genome assembly. Genomic regions of low within-group variation are remarkably consistent between the three populations. These regions show high relative differentiation but low absolute differentiation between populations. Comparisons with outgroup species show the locations of these peaks of relative differentiation are not well explained by phylogenetically conserved variation in recombination rates or selection. These patterns are consistent with a model in which selection in an ancestral form has reduced variation at some parts of the genome, and those same regions experience recurrent selection that subsequently reduces variation within each subspecies. The degree of heterogeneity in nucleotide diversity is greater than explained by models of background selection, but is consistent with selective sweeps. Given the evidence that greenish warblers have had both population differentiation for a long period of time and periods of gene flow between those populations, we propose that some genomic regions underwent selective sweeps over a broad geographic area followed by within-population selection-induced reductions in variation. An important implication of this ‘sweep-before-differentiation’ model is that genomic regions of high relative differentiation may have moved among populations more recently than other genomic regions.
Congrats to coauthors Christine Grossen, Sampath Seneviratne, and Daniel Croll on our publication about genomic variation in three species of sapsuckers and two hybrid zones.
The paper: Grossen, C., S.S. Seneviratne, D. Croll, and D.E. Irwin. 2016. Strong reproductive isolation and narrow genomic tracts of differentiation among three woodpecker species in secondary contact. Molecular Ecology, online Early View: doi:10.1111/mec.13751 Link
The Abstract: Hybrid zones allow the measurement of gene flow across the genome, producing insight into the genomic architecture of speciation. Such analysis is particularly powerful when applied to multiple pairs of hybridizing species, as patterns of genomic differentiation can then be related to age of the hybridizing species, providing a view into the build-up of differentiation over time. We examined 33 809 single nucleotide polymorphisms (SNPs) in three hybridizing woodpecker species: Red-breasted, Red-naped and Yellow-bellied sapsuckers (Sphyrapicus ruber, Sphyrapicus nuchalis and Sphyrapicus varius), two of which (ruber and nuchalis) are much more closely related than each is to the third (varius). To identify positions of SNPs on chromosomes, we developed a localization method based on comparative genomics. We found narrow clines, bimodal distributions of hybrid indices and genomic regions with decreased rates of introgression. These results suggest moderately strong reproductive isolation among species and selection against specific hybrid genotypes. We found 19 small regions of strong differentiation between species, partly shared among species pairs, but no large regions of differentiation. An association analysis revealed a single strong-effect candidate locus associated with plumage, possibly explaining mismatch among the three species in genomic relatedness and plumage similarity. Our comparative analysis of species pairs of different age and their hybrid zones showed that moderately strong reproductive isolation can occur with little genomic differentiation, but that reproductive isolation is incomplete even with much greater genomic differentiation, implying there are long periods of time when hybridization is possible if diverging populations are in geographic contact.
Congrats to coauthors Dave Toews, Alan Brelsford, Christine Grossen, and Borja Milá on our publication of patterns of genomic variation within and among four forms of yellow-rumped warblers:
Toews, D.P.L., A. Brelsford, B. Milá, C. Grossen, and D.E. Irwin. 2016. Genomic variation across the yellow-rumped warbler species complex. The Auk: Ornithological Advances 133: 698-717. Link
Populations that have experienced long periods of geographic isolation will diverge over time. The application of high-throughput sequencing technologies to study the genomes of related taxa now allows us to quantify, at a fine scale, the consequences of this divergence across the genome. Throughout a number of studies, a notable pattern has emerged. In many cases, estimates of differentiation across the genome are strongly heterogeneous; however, the evolutionary processes driving this striking pattern are still unclear. Here we quantified genomic variation across several groups within the Yellow-rumped Warbler species complex (Setophaga spp.), a group of North and Central American wood warblers. We showed that genomic variation is highly heterogeneous between some taxa and that these regions of high differentiation are relatively small compared to those in other study systems. We found that the clusters of highly differentiated markers between taxa occur in gene-rich regions of the genome and exhibit low within-population diversity. We suggest these patterns are consistent with selection, shaping genomic divergence in similar genomic regions across the different populations. Our study also confirms previous results relying on fewer genetic markers that several of the phenotypically distinct groups in the system are also genomically highly differentiated, likely to the point of full species status.