Congrats to Madelyn (“Maddie”) Ore and Silu Wang for their publication on song and genetic variation in coastal vs. inland populations of Setophaga townsendi. Maddie did her MSc research on this project in our lab, and is now a PhD candidate at Cornell University.

The full citation:
Ore, M.J., S. Wang, and D. Irwin. 2023. Gradual transitions in genetics and songs between coastal and inland populations of Setophaga townsendi. Ornithology 140(2:April): 1-14. https://doi.org/10.1093/ornithology/ukac060

The abstract:
Setophaga townsendi is a species of wood warbler (family Parulidae) in northwestern North America that has geographic structure in the mitochondrial and nuclear genomes: while interior populations have differentiated mitonuclear ancestry from the sister species S. occidentalis, coastal populations have a mix of inland and S. occidentalis mitonuclear ancestries. This coastal to inland transition in genomic ancestry raises the possibility of similar geographic structure in phenotypic traits, especially those involved in mate choice. Using qualitative and multivariate approaches, we investigated whether there is a sharp transition between coastal and inland populations in both song and in nuclear DNA. We find there is a shallow geographic cline in Type I song but not in Type II song. Nuclear DNA shows a gradient between coast and inland. There is little correlation between variation in song and the isolation-by-distance pattern in the nuclear DNA. Learned songbird song is shaped by both genetic and cultural processes. There has been a debate on whether song learning promotes or slows down population differentiation. By comparing the within-species variation in song and genetic structures, we can expand our understanding of the dynamic interplay between mating signals and population differentiation.

Ethical note:
This species desperately needs a new official English name. Hence we made this comment in the paper: “We refrained from using the existing common name for Setophaga townsendi in support of the Bird Names for Birds Movement.” To learn more about why, click on this Bird Names for Birds historical bio.

Congrats to Libby Natola on the publication of her paper comparing hybridization dynamics among three well-separated transects across the Red-breasted / Red-naped Sapsucker hybrid zone!

Fig. 1 of the paper:

The full citation:
Natola, L., S.M. Billerman, M.D. Carling, S.S. Seneviratne, and D. Irwin. 2023. Geographic variability of hybridization between red-breasted and red-naped sapsuckers. Evolution 77: 580-592. Link

The abstract:
Hybrid zones reveal the strength of reproductive isolation between populations undergoing speciation and are a key tool in evolutionary biology research. Multiple replicate transects across the same hybrid zone offer insight into the dynamics of hybridization in different environments, clarifying the role of extrinsic forces on the speciation process. Red-breasted and red-naped sapsuckers (Sphyrapicus ruber and Sphyrapicus nuchalis) have a long zone of contact over approximately 1,600 km from central British Columbia, Canada to central California, USA. We used Genotyping-by-Sequencing data from three independent sapsucker hybrid zone transects to compare hybridization dynamics between these species under variable geoclimatic conditions. We generated geographic clines of the genomic data to compare hybrid zone widths and used random forests models and linear regression to assess the relationship between climate and sapsucker ancestry along each transect. Our results show variation in the directionality of backcrossing, often indicative of moving hybrid zones. We note variable cline widths among transects, indicating differences in selection maintaining hybrid zone dynamics. Furthermore, random forests models identified different variables in close association with sapsucker ancestry across each transect. These results indicate a lack of repeatability across replicate transects and a strong influence of the local environment on hybrid zone dynamics.

We thank collaborators and coauthors Shawn Billerman, Matt Carling, and Sampath Seneviratne for their excellent contributions to this project.

We are celebrating Libby Natola’s outstanding PhD dissertation defence on Dec. 6th. Libby’s examining committee was unanimously impressed with the quality of her research and dissertation.

Dr. Natola’s dissertation is titled “Reproductive Isolation among Sphyrapicus Sapsuckers” and consists of four research chapters. One of these is published and one is in press:

Natola, L., S.S. Seneviratne, and D. Irwin. 2022. Population genomics of an emergent tri-species hybrid zone. Molecular Ecology 31: 5356-5367. Link

Natola, L., S.M. Billerman, M.D. Carling, S.S. Seneviratne, and D. Irwin. In press. Geographic variability of hybridization between red-breasted and red-naped sapsuckers. Evolution, in press. (earlier version posted on bioRxiv: Link )

Two more are on the way!

It has been a pleasure to work with Libby, and we send her forth with very best wishes.

Congrats to graduated MSc student Ellen Nikelski (now PhD student, University of Toronto) on the publication of her paper on co-introgression of mitochondrial and nuclear genes between Pine Buntings and Yellowhammers.

Fig. 1 from the paper:

The full citation:
Nikelski, E., A.S. Rubtsov, and D. Irwin. 2022. High heterogeneity in genomic differentiation between phenotypically divergent songbirds: a test of mitonuclear co-introgression. Heredity, published online at https://doi.org/10.1038/s41437-022-00580-8

The abstract:
Comparisons of genomic variation among closely related species often show more differentiation in mitochondrial DNA (mtDNA) and sex chromosomes than in autosomes, a pattern expected due to the differing effective population sizes and evolutionary dynamics of these genomic components. Yet, introgression can cause species pairs to deviate dramatically from general differentiation trends. The yellowhammer (Emberiza citrinella) and pine bunting (E. leucocephalos) are hybridizing avian sister species that differ greatly in appearance and moderately in nuclear DNA, but that show no mtDNA differentiation. This discordance is best explained by adaptive mtDNA introgression—a process that can select for co-introgression at nuclear genes with mitochondrial functions (mitonuclear genes). To better understand these discordant differentiation patterns and characterize nuclear differentiation in this system, we investigated genome-wide differentiation between allopatric yellowhammers and pine buntings and compared it to what was seen previously in mtDNA. We found significant nuclear differentiation that was highly heterogeneous across the genome, with a particularly wide differentiation peak on the sex chromosome Z. We further investigated mitonuclear gene co-introgression between yellowhammers and pine buntings and found support for this process in the direction of pine buntings into yellowhammers. Genomic signals indicative of co-introgression were common in mitonuclear genes coding for subunits of the mitoribosome and electron transport chain complexes. Such introgression of mitochondrial DNA and mitonuclear genes provides a possible explanation for the patterns of high genomic heterogeneity in genomic differentiation seen among some species groups.

Congrats to PhD Candidate Libby Natola on the publication of her paper on three-species hybridization in sapsuckers!

Figs.1 & 2 from the paper:

The full citation:
Natola, L., S.S. Seneviratne, and D. Irwin. 2022. Population genomics of an emergent tri-species hybrid zone. Molecular Ecology, early view: https://doi.org/10.1111/mec.16650
(earlier version posted on bioRxiv: Link )

The abstract:
Isolating barriers that drive speciation are commonly studied in the context of two-species hybrid zones. There is however evidence that more complex introgressive relationships are common in nature. Here, we use field observations and genomic analysis, including the sequencing and assembly of a novel reference genome, to study an emergent hybrid zone involving two colliding hybrid zones of three woodpecker species: Red-breasted, Red-naped, and Yellow-bellied Sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius). Surveys of the area surrounding Prince George, British Columbia, Canada, show that all three species are sympatric, and Genotyping-by-Sequencing identifies hybrids from each species pair and birds with ancestry from all three species. Observations of mate pair phenotypes and genotypes provide evidence for assortative mating, though there is some heterospecific pairing. Hybridization is more extensive in this tri-species hybrid zone than in two di-species hybrid zones. However, there is no evidence of a hybrid swarm and admixture is constrained to contact zones, so we classify this region as a tension zone and invoke selection against hybrids as a likely mechanism maintaining species boundaries. Analysis of sapsucker age classes does not show disadvantages in hybrid survival to adulthood, so we speculate the selection upholding the tension zone may involve hybrid fecundity. Gene flow among all sapsuckers in di-species hybrid zones suggests introgression likely occurred before the formation of this tri-species hybrid zone, and might result from bridge hybridization, vagrancies, or other three-species interactions.

The full citation:
Irwin, D., and D. Schluter. 2022. Hybridization and the coexistence of species. American Naturalist 200(3): Ahead of Print. https://doi.org/10.1086/720365 (earlier version posted on bioRxiv: Link )

The abstract:
It is thought that two species can coexist if they use different resources present in the environment, yet this assumes that species are completely reproductively isolated. We model coexistence outcomes for two sympatric species that are ecologically differentiated but have incomplete reproductive isolation. The consequences of interbreeding depend crucially on hybrid fitness. When hybrid fitness is high, just a small rate of hybridization can lead to collapse of two species into one. Low hybrid fitness can cause population declines, making extinction of one or both species likely. High intrinsic growth rates result in higher reproductive rates when populations are below carrying capacity, reducing the probability of extinction and increasing the probability of stable coexistence at moderate levels of assortative mating and hybrid fitness. Very strong but incomplete assortative mating can induce low hybrid fitness via a mating disadvantage to rare genotypes, and this can stabilize coexistence of two species at high but incomplete levels of assortative mating. Given these results and evidence that it may take many millions of years of divergence before related species become sympatric, we postulate that coexistence of closely-related species is more often limited by insufficient assortative mating than by insufficient ecological differentiation.

A 10-minute talk (from the Evolution conference in 2021) summarizing the paper:

Congratulations to lead author Dr. Silu Wang and coauthors on the publication of a paper on the history and genomic makeup of coastal populations of Setophaga townsendi, pictured here (photo by D. Irwin):

Silu and I are grateful for the contributions of coauthors Maddie Ore, Else Mikkelsen, Julie Lee-Yaw, David Toews, and Sievert Rohwer.

The full citation:
Wang, S., M.J. Ore, E.K. Mikkelsen, J. Lee-Yaw, D.P.L. Toews, S. Rohwer, and D. Irwin. 2021. Signatures of mitonuclear coevolution in a warbler species complex. Nature Communications 12: 4279. https://doi.org/10.1038/s41467-021-24586-8

The abstract:
Divergent mitonuclear coadaptation could facilitate speciation. We investigate this possibility in two hybridizing species of warblers, Setophaga occidentalis and S. townsendi, in western North America. Inland S. townsendi harbor distinct mitochondrial DNA haplotypes from those of S. occidentalis. These populations also differ in several nuclear DNA regions. Coastal S. townsendi demonstrate mixed mitonuclear ancestry from S. occidentalis and inland S. townsendi. Of the few highly-differentiated chromosomal regions between inland S. townsendi and S. occidentalis, a 1.2 Mb gene block on chromosome 5 is also differentiated between coastal and inland S. townsendi. Genes in this block are associated with fatty acid oxidation and energy-related signaling transduction, thus linked to mitochondrial functions. Genetic variation within this candidate gene block covaries with mitochondrial DNA and shows signatures of divergent selection. Spatial variation in mitonuclear ancestries is correlated with climatic conditions. Together, these observations suggest divergent mitonuclear coadaptation underpins cryptic differentiation in this species complex.

Below is figure 1 from the paper, showing Silu’s beautiful graphics, and you can see more interesting figures here.

Congratulations to Else Mikkelsen on the publication of her excellent Honours Thesis work on genomic differentiation between Pacific and Winter Wrens.

The full citation:
Mikkelsen, E.K., and D. Irwin. 2021. Ongoing production of low-fitness hybrids limits range overlap between divergent cryptic species. Molecular Ecology, online early view: https://doi.org/10.1111/mec.16015 .

The abstract:
Contact zones between recently diverged taxa provide opportunities to examine the causes of reproductive isolation and the processes that determine whether two species can coexist over a broad region. The Pacific wren (Troglodytes pacificus) and winter wren (Troglodytes hiemalis) are two morphologically similar songbirds that started diverging about 4 million years ago, older than most sister species pairs of temperate songbirds. The ranges of these species come into narrow contact in western Canada, where the two species remain distinct. To assess evidence for differentiation, hybridization and introgression in this system, we examined variation in over 250,000 single nucleotide polymorphism markers distributed across the genome. The two species formed highly divergent genetic clusters, consistent with long-term differentiation. In a set of 75 individuals, two first-generation hybrids (i.e., F₁’s) were detected, indicating only moderate levels of assortative mating between these taxa. We found no recent backcrosses or other evidence of recent breeding success of F₁’s, indicating very low or zero fitness of F₁ hybrids. Examination of genomic variation shows evidence for only a single backcrossing event many generations ago. The moderate rate of hybridization combined with very low F₁ hybrid fitness is expected to result in a population sink in the contact zone, largely explaining the narrow overlap of the two species. If such dynamics are common in nature, they could explain the narrow range overlap often observed between pairs of closely related species.

To read a Twitter thread about the paper, click here.

Congratulations to lead author Dr. Silu Wang who has published another excellent paper on the hybrid zone between two beautiful warbler species, Setophaga occidentalis (Hermit Warbler) and Setophaga townsendi. Here is Silu’s beautiful painting inspired by the hybrid zone:

Silu and I are grateful to the contributions of coauthors Sievert Rohwer, Devin de Zwaan, David Toews, Irby Lovette, and Jacqueline Mackenzie.

The full citation:
Wang, S., S. Rohwer, D.R. de Zwaan, D.P.L. Toews, I.J. Lovette, J. Mackenzie, and D. Irwin. 2020. Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species. Evolution Letters, online Early View; https://doi.org/10.1002/evl3.198

The abstract:
Speciation is one of the most important processes in biology, yet the study of the genomic changes underlying this process is in its infancy. North American warbler species Setophaga townsendi and Setophaga occidentalis hybridize in a stable hybrid zone, following a period of geographic separation. Genomic differentiation accumulated during geographic isolation can be homogenized by introgression at secondary contact, whereas genetic regions that cause low hybrid fitness can be shielded from such introgression. Here, we examined the genomic underpinning of speciation by investigating (1) the genetic basis of divergent pigmentation traits between species, (2) variation in differentiation across the genome, and (3) the evidence for selection maintaining differentiation in the pigmentation genes. Using tens of thousands of single nucleotide polymorphisms (SNPs) genotyped in hundreds of individuals within and near the hybrid zone, genome‐wide association mapping revealed a single SNP associated with cheek, crown, breast coloration, and flank streaking, reflecting pleiotropy (one gene affecting multiple traits) or close physical linkage of different genes affecting different traits. This SNP is within an intron of the RALY gene, hence we refer to it as the RALY SNP. We then examined between‐species genomic differentiation, using both genotyping‐by‐sequencing and whole genome sequencing. We found that the RALY SNP is within one of the highest peaks of differentiation, which contains three genes known to influence pigmentation: ASIP, EIF2S2, and RALY (the ASIP‐RALY gene block). Heterozygotes at this gene block are likely of reduced fitness, as the geographic cline of the RALY SNP has been narrow over two decades. Together, these results reflect at least one barrier to gene flow within this narrow (∼200 kb) genomic region that modulates plumage difference between species. Despite extensive gene flow between species across the genome, this study provides evidence that selection on a phenotype‐associated genomic region maintains a stable species boundary.

To read a Twitter thread about the paper, click here.

To read Silu’s blog about this paper on the Evolution Letters website, click here.