Congratulations to lead author Ellen Nikelski and collaborator Alex Rubtsov on today’s publication of this Molecular Ecology paper:

Nikelski, E., A.S. Rubtsov, and D. Irwin. 2024. A sex chromosome polymorphism maintains divergent plumage phenotypes between extensively hybridizing yellowhammers (Emberiza citrinella) and pine buntings (E. leucocephalos). Molecular Ecology, Early View: https://doi.org/10.1111/mec.17526

The paper shows that the divergent plumages of these two species and their hybrids are largely associated with two distinct types of Z chromosomes (a sex chromosome):

The abstract:
Under allopatric speciation, populations of a species become isolated by a geographic barrier and develop reproductive isolation through genetic differentiation. When populations meet in secondary contact, the strength of evolved reproductive barriers determines the extent of hybridization and whether the populations will continue to diverge or merge together. The yellowhammer (Emberiza citrinella) and pine bunting (E. leucocephalos) are avian sister species that diverged in allopatry on either side of Eurasia during the Pleistocene glaciations. Though they differ greatly in plumage and form distinct genetic clusters in allopatry, these taxa show negligible mitochondrial DNA differentiation and hybridize extensively where they overlap in central Siberia, lending uncertainty to the state of reproductive isolation in the system. To assess the strength of reproductive barriers between taxa, we examined genomic differentiation across the system. We found that extensive admixture has occurred in sympatry, indicating that reproductive barriers between taxa are weak. We also identified a putative Z chromosome inversion region that underlies plumage variation in the system, with the ‘pine bunting’ haplotype showing dominance over the ‘yellowhammer’ haplotype. Our results suggest that yellowhammers and pine buntings are currently at a crossroads and that evolutionary forces may push this system towards either continued differentiation or population merging. However, even if these taxa merge, recombination suppression between putative chromosome Z inversion haplotypes may maintain divergent plumage phenotypes within the system. In this way, our findings highlight the important role hybridization plays in increasing the genetic and phenotypic variation as well as the evolvability of a system.

This is the second paper from Ellen’s MSc thesis. Ellen is now a PhD student in Jason Weir’s group at the University of Toronto Scarborough.

Congratulations to lead author Quinn McCallum on today’s publication of his paper on genomic differentiation of Zonotrichia sparrows in the Journal of Evolutionary Biology. Quinn conducted this work while an Honours undergraduate student at UBC. Quinn and I are also grateful for the contributions of coauthors Kenny Askelson, Finola Fogarty, Libby Natola, Ellen Nikelski, and Andrew Huang. We also thank WildResearch and the Iona Island Bird Observatory for their contributions to the study.

The abstract:
When a single species evolves into multiple descendent species, some parts of the genome can play a key role in the evolution of reproductive isolation while other parts flow between the evolving species via interbreeding. Genomic evolution during the speciation process is particularly interesting when major components of the genome—for instance, sex chromosomes vs. autosomes vs. mitochondrial DNA—show widely differing patterns of relationships between three diverging populations. The golden-crowned sparrow (Zonotrichia atricapilla) and the white-crowned sparrow (Zonotrichia leucophrys) are phenotypically differentiated sister species that are largely reproductively isolated despite possessing similar mitochondrial genomes, likely due to recent introgression. We assessed variation in more than 45,000 single nucleotide polymorphisms to determine the structure of nuclear genomic differentiation between these species and between two hybridizing subspecies of Z. leucophrys. The two Z. leucophrys subspecies show moderate levels of relative differentiation and patterns consistent with a history of recurrent selection in both ancestral and daughter populations, with much of the sex chromosome Z and a large region on the autosome 1A showing increased differentiation compared to the rest of the genome. The two species Z. leucophrys and Z. atricapilla show high relative differentiation and strong heterogeneity in the level of differentiation among various chromosomal regions, with a large portion of the sex chromosome (Z) showing highly divergent haplotypes between these species. Studies of speciation often emphasize mitochondrial DNA differentiation, but speciation between Z. atricapilla and Z. leucophrys appears primarily associated with Z chromosome divergence and more moderately associated with autosomal differentiation, whereas mitochondria are highly similar due apparently to recent introgression. These results add to the growing body of evidence for highly heterogeneous patterns of genomic differentiation during speciation, with some genomic regions showing a lack of gene flow between populations many hundreds of thousands of years before other genomic regions.

The citation:
McCallum, Q., K. Askelson, F.F. Fogarty, L. Natola, E. Nikelski, A. Huang, and D. Irwin. 2024. Pronounced differentiation on the Z chromosome and parts of the autosomes in crowned sparrows contrasts with mitochondrial paraphyly: implications for speciation. Journal of Evolutionary Biology, voae004, https://doi.org/10.1093/jeb/voae004

Quinn is now a PhD student in the Mason Lab at Louisiana State University. You can learn more about him and his work here.

Kenny’s PhD defence last week went super well, and we are pleased to announce Dr. Kenneth Askelson!

Dr. Askelson’s dissertation is titled “Introgression, recombination, and genomic differentiation in a cryptic species complex of North American passerines.”

This week we are also celebrating the publishing of one of Kenny’s papers:

Askelson, K., G.M. Spellman, and D. Irwin. 2023. Genomic divergence and introgression between cryptic species of a widespread North American songbird. Molecular Ecology 32: 6839-6853. Link

Congrats Kenny!!

The journal Heredity, the journal of the Genetics Society, has awarded Ellen Nikelski their Best Student Paper 2023 prize, for her paper “High heterogeneity in genomic differentiation between phenotypically divergent songbirds: a test of mitonuclear co-introgression.” Ellen’s research for this paper was conducted while an MSc student at UBC, and she is now a PhD student at the University of Toronto.

To learn more, see: https://www.nature.com/collections/hjgfdeeige

Nikelski, E., A.S. Rubtsov, and D. Irwin. 2023. High heterogeneity in genomic differentiation between phenotypically divergent songbirds: a test of mitonuclear co-introgression. Heredity 130: 1-13. Link

Congratulations to Ellen on this well-deserved award!!

Today, Molecular Ecology published Kenny’s paper that provides genomic evidence of 3-4 cryptic species of White-breasted Nuthatch, as well as introgression from a ghost lineage.

The Abstract:
Analysis of genomic variation among related populations can sometimes reveal distinct species that were previously undescribed due to similar morphological appearances, and close examination of such cases can provide much insight regarding speciation. Genomic data can also reveal the role of reticulate evolution in differentiation and speciation. White-breasted nuthatches (Sitta carolinensis) are widely distributed North American songbirds that are currently classified as a single species but have been suspected to represent a case of cryptic speciation. Previous genetic analyses suggested four divergent groups, but it was unclear whether these represented multiple reproductively isolated species. Using extensive genomic sampling of over 350 white-breasted nuthatches from across North America and a new chromosome-level reference genome, we asked if white-breasted nuthatches are comprised of multiple species and whether introgression has occurred between divergent populations. Genomic variation of over 300,000 loci revealed four highly differentiated populations (Pacific, n = 45; Eastern, n = 23; Rocky Mountains North, n = 138; and Rocky Mountains South, n = 150) with geographic ranges that are adjacent. We observed a moderate degree of admixture between Rocky Mountain populations but only a small number of hybrids between the Rockies and the Eastern population. The rarity of hybrids together with high levels of differentiation between populations is supportive of populations having some level of reproductive isolation. Between populations, we show evidence for introgression from a divergent ghost lineage of white-breasted nuthatches into the Rocky Mountains South population, which is otherwise closely related to Rocky Mountains North. We conclude that white-breasted nuthatches are best considered at least three species and that ghost lineage introgression has contributed to differentiation between the two Rocky Mountain populations. White-breasted nuthatches provide a dramatic case of morphological similarity despite high genomic differentiation, and the varying levels of reproductive isolation among the four groups provide an example of the speciation continuum.

Kenny and I are grateful for the collaboration of Garth Spellman on this project.

The citation:
Askelson, K., G.M. Spellman, and D. Irwin. 2023. Genomic divergence and introgression between cryptic species of a widespread North American songbird. Molecular Ecology, Early View, https://doi.org/10.1111/mec.17169

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.