Biology subjects

Irwin, D. E.

Publications and source records attributed to Irwin, D. E..

9 recordsLinked to original sources

bioRxiv2023

Evidence for ancient selective sweeps followed by differentiation among three species of Sphyrapicus sapsuckers

Speciation occurs when gene pools differentiate between populations, but that differentiation is often highly heterogeneous across the genome. Understanding what parts of the genome are more prone to differentiation can inform us about genomic regions and evolutionary processes that may be central to the speciation process. Here, we study genomic variation among three hybridizing species of North American woodpecker: red-breasted, red-naped, and yellow-bellied sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius). We use whole genome resequencing to measure genetic variation among these species and to quantify how the level of differentiation varies across the genome. We find that regions of high relative differentiation between species (FST) tend to have low absolute differentiation between species ({pi}B), indicating that regions of high relative differentiation often have more recent between-population coalescence times than regions of low relative differentiation do. Most of the high-FST genomic windows are found on the Z chromosome, indicating this sex chromosome is particularly important in sapsucker differentiation and potentially speciation. These results are consistent with a model of speciation in which selective sweeps of globally advantageous variants spread among partly differentiated populations, followed by differential local adaptation of those same genomic regions. We propose that sapsucker speciation may have occurred primarily via this process occurring on the Z chromosomes, resulting in genetic incompatibilities involving divergent Z chromosomes.

evolutionary biology↗

bioRxiv2022

Extreme sex chromosome differentiation, likely driven by inversion, contrasts with mitochondrial paraphyly between species of crowned sparrows

Sympatric species pairs provide researchers with the opportunity to study patterns of genomic differentiation during the late stages of speciation and to identify the genomic regions underlying reproductive isolation. The Golden-crowned Sparrow (Zonotrichia atricapilla) and the White-crowned Sparrow (Zonotrichia leucophrys) are broadly sympatric songbirds found in western North America. These sister species are phenotypically differentiated and largely reproductively isolated despite possessing similar mitochondrial genomes, likely due to recent mitochondrial introgression. We used a genotyping-by-sequencing (GBS) approach to determine the structure of nuclear genomic differentiation between these species and also between two hybridizing subspecies of Z. leucophrys, across more than 45,000 single nucleotide polymorphisms (SNPs). The two Z. leucophrys subspecies showed moderate levels of relative differentiation, as well as patterns consistent with a history of recurrent selection in both ancestral and daughter populations. Z. leucophrys and Z. atricapilla show high levels of relative differentiation and strong heterogeneity in the level of differentiation among different chromosomal regions, with a large portion of the Z chromosome showing highly elevated differentiation. Patterns of relative and absolute differentiation and linkage disequilibrium suggest a large inversion on the Z chromosome, with inversion haplotypes that segregate between Z. atricapilla and Z. leucophrys. While mitochondrial DNA differentiation is often emphasized in studies of speciation, differentiation between these Zonotrichia sparrows appears to have occurred first in the Z chromosome and secondarily in autosomes, followed by mitochondrial introgression. This putative inversion has implications for reproductive isolation between these species and adds to a growing body of evidence for the importance of inversions and the Z chromosome in speciation.

evolutionary biology↗

bioRxiv2022

Population genomics of an emergent tri-species hybrid zone

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.

evolutionary biology↗

bioRxiv2021

Ongoing production of low-fitness hybrids limits range overlap between divergent cryptic species

Contact zones between recently-diverged taxa provide opportunities to examine the causes of reproductive isolation and to examine the processes that determine whether two species can coexist over a broad region. The Pacific Wren (Troglodytes pacificus) and the Winter Wren (Troglodytes hiemalis) are two morphologically similar songbird species that started diverging about 4 million years ago, older than most sister species pairs. The ranges of these species come into narrow contact in western Canada, where the two species remain distinct in sympatry. 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 genomes of the two species. The two species formed highly divergent genetic clusters, consistent with long-term differentiation. In a set of 75 individuals from allopatry and sympatry, two first-generation hybrids (i.e., F1s) were detected, indicating only moderate levels of assortative mating between these taxa. We found no recent backcrosses or F2s or other evidence of recent breeding success of F1 hybrids, indicating very low or zero fitness of F1 hybrids. Examination of genomic variation shows evidence for only a single backcrossing event in the distant past. The sizeable rate of hybridization combined with very low fitness of F1 hybrids 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. Additionally, we present evidence for a rare duplication of a large chromosomal segment from an autosome to the W chromosome, the female-specific sex chromosome in birds.

evolutionary biology↗

bioRxiv2020

Signatures of mito-nuclear climate adaptation in a warbler species complex

Mitochondrial (mtDNA) and nuclear (nDNA) genes interact to govern metabolic pathways of mitochondria. When differentiated populations interbreed at secondary contact, incompatibilities between mtDNA of one population and nDNA of the other could result in low fitness of hybrids. In northwestern North America, two hybridizing species of warblers, Setophaga occidentalis (abbreviated as SOCC) and S. townsendi (STOW), provide an excellent system to investigate the potential co-adaptation of mitochondrial and nuclear DNA. The inland population of STOW (inland STOW) harbors mtDNA haplotype that is half a million years divergent from the SOCC mtDNA, and these populations also differ strongly in a few nDNA regions. Coastal populations of STOW (coastal STOW) have mixed ancestry, consistent with ancient hybridization of SOCC and inland STOW-like population. Of the few highly-differentiated nDNA regions between inland STOW and SOCC, one of these regions (on chromosome 5) is also differentiated between coastal STOW and inland STOW, and covaries with mtDNA among coastal STOW populations. Genes in this 1.2Mb region of chromosome 5 are associated with fatty acid oxidation and energy-related signaling transduction, both of which are closely associated with mitochondrial function. This chromosome 5 region is correlated with mtDNA haplotypes both within and across sampling sites, a pattern consistent with mitonuclear co-adaptation. We show that such mitonuclear coevolution might be maintained by climate-related selection, because mitonuclear ancestry is correlated with climatic conditions among sampling sites. Together, our observation suggests climatic-associated adaptation shaping mitonuclear differentiation and introgression in this species complex.

evolutionary biology↗

bioRxiv2019

Selection on a pleiotropic color gene block underpins early differentiation between two warbler species

When one species gradually splits into two, divergent selection on specific traits can cause peaks of differentiation in the genomic regions encoding those traits. Whether speciation is initiated by strong selection on a few genomic regions with large effects or by more diffused selection on many regions with small effects remains controversial. Differentiated phenotypes between differentiating lineages are commonly involved in reproductive isolation, thus their genetic underpinnings are key to the genomics architecture of speciation. When two species hybridize, recombination over multiple generations can help reveal the genetic regions responsible for the differentiated phenotypes against a genomic background that has been homogenized via backcrossing and introgression. We used admixture mapping to investigate genomic differentiation and the genetic basis of differentiated plumage features (relative melanin and carotenoid pigment) between hybridizing sister species in the early stage of speciation: Townsends (Setophaga townsendi) and Hermit warblers (S. occidentalis). We found a few narrow and dispersed divergent regions between allopatric parental populations, consistent with the divergence with gene flow model of speciation. One of the divergent peaks involves three genes known to affect pigmentation: ASIP, EIF2S2, and RALY (the ASIP-RALY gene block). After controlling for population substructure, we found that a single nucleotide polymorphism (SNP) inside the intron of RALY displays a strong pleiotropic association with cheek, crown, and breast coloration. In addition, we detect selection on the ASIP-RALY gene block, as the geographic cline of the RALY marker of this gene block has remained narrower than the plumage cline, which remained narrower than expected under neutral diffusion over two decades. Despite extensive gene flow between these species across much of the genome, the selection on ASIP-RALY gene block maintains stable genotypic and plumage difference between species allowing further differentiation to accumulate via linkage to its flanking genetic region or linkage-disequilibrium genome-wide.

evolutionary biology↗

bioRxiv2019

Assortative mating in hybrid zones is remarkably ineffective in promoting speciation

Assortative mating and other forms of partial prezygotic isolation are often viewed as being more important than partial postzygotic isolation (low fitness of hybrids) early in the process of speciation. Here I simulate secondary contact between two populations ( species) to examine effects of pre- and postzygotic isolation in preventing blending. A small reduction in hybrid fitness (e.g., 10%) produces a narrower hybrid zone than a strong but imperfect mating preference (e.g., 10x stronger preference for conspecific over heterospecific mates). This is because, in the latter case, rare F1 hybrids find each other attractive (due to assortative mating), leading to the gradual buildup of a full continuum of intermediates between the two species. The cline is narrower than would result from purely neutral diffusion over the same number of generations, largely due to the frequency-dependent mating disadvantage of individuals of rare mating types. Hybrids tend to pay this cost of rarity more than pure individuals, meaning there is an induced postzygotic isolation effect of assortative mating. These results prompt a questioning of the concept of partial prezygotic isolation, since it is not very isolating unless there is also postzygotic isolation.

evolutionary biology↗

bioRxiv2018

Population genomic analyses reveal a highly differentiated genetic cluster of northern goshawks (Accipiter gentilis laingi) in Haida Gwaii

Accurate knowledge of geographic ranges and genetic relationships among populations is important when managing a species or population of conservation concern. In the western Canadian province of British Columbia, a subspecies of the northern goshawk (Accipiter gentilis laingi) is designated as Threatened under the Canadian Species at Risk Act. Historically, the range of this bird of prey has been ambiguous and its genetic distinctness from the other North American subspecies (Accipiter gentilis atricapillus) has not been well established. Given the uncertainty in using morphological traits to assign individual goshawks to these two subspecies, we analyzed genomic relationships in tens of thousands of single nucleotide polymorphisms identified using genotyping-bysequencing of high-quality genetic samples. This genome-wide analysis revealed a genetically distinct population of northern goshawks on the archipelago of Haida Gwaii and subtle genetic structuring among the remainder of our sampling sites within North America. Following from this analysis, we developed targeted genotyping assays for ten loci that are highly differentiated between the two main genetic clusters, allowing the addition of hundreds of low-quality samples to our analysis. This additional information confirmed that the distinct genetic cluster on Haida Gwaii is restricted to that archipelago. As the laingi form was originally described as being based in Haida Gwaii, where the type specimen of that form is from, further study (especially of morphological traits) may indicate a need to restrict this name to the Haida Gwaii genetic cluster. Regardless of taxonomic treatment, our finding of a distinct Haida Gwaii genetic cluster along with the small and historically declining population size of the Haida Gwaii population suggests a high risk of extinction of an ecologically and genetically distinct form of northern goshawk. Outside of Haida Gwaii, sampling regions along the coast of BC and southeast Alaska (often considered regions inhabited by laingi) show some subtle differentiation from other North American regions. We anticipate that these results will increase the effectiveness of conservation management of northern goshawks in northwestern North America. More broadly, other conservation-related studies of genetic variation may benefit from the two-step approach we employed that first surveys genomic variation using high-quality samples and then genotypes low-quality samples at particularly informative loci.

genomics↗

bioRxiv2017

Comparative analysis examining patterns of genomic differentiation across multiple episodes of population divergence in birds

Heterogeneous patterns of genomic differentiation are commonly documented between closely related populations and there is considerable interest in identifying factors that contribute to their formation. These factors could include genomic features (e.g., areas of low recombination) that promote processes like linked selection (positive or purifying selection that affects linked neutral sites) at specific genomic regions. Examinations of repeatable patterns of differentiation across population pairs can provide insight into the role of these factors. Birds are well suited for this work, as genome structure is conserved across this group. Accordingly, we re-estimated relative (FST) and absolute (dXY) differentiation between eight sister pairs of birds that span a broad taxonomic range using a common pipeline. Across pairs, there were modest but significant correlations in window-based estimates of differentiation (up to 3% of variation explained for FST and 26% for dXY), supporting a role for processes at conserved genomic features in generating heterogeneous patterns of differentiation. This suggestion was reinforced by linear models identifying several genomic features (e.g., gene densities) as significant predictors of FST and dXY repeatability. FST repeatability was higher among pairs that were further along the speciation continuum (i.e., more reproductively isolated), suggesting that early stages of speciation may be dominated by positive selection that is different between pairs and replaced by processes acting according to shared genomic features as speciation proceeds.

genomics↗