Darren Irwin

Professor

Research Classification

Research Interests

evolutionary genetics
genomic differentiation
hybridization
ornithology
seasonal migration
speciation

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I am interested in and conduct interdisciplinary research.
 
 

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Genomics
DNA Sequencing
bioacoustics
field research
bioinformatics

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Please see: https://www.zoology.ubc.ca/~irwin/irwinlab/

 

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Graduate Student Supervision

Doctoral Student Supervision

Dissertations completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest dissertations.

Introgression, recombination, and genomic differentiation in a cryptic species complex of North American passerines (2024)

Understanding how selection, recombination, and introgression interact during the speciationprocess is a key goal in the field of evolution, and many questions remain unanswered. In mydissertation, I make use of a cryptic species complex of white-breasted nuthatches (Sittacarolinensis) to understand the landscape of genomic differentiation between these putativespecies and how recombination and introgression have shaped those patterns. I then extend myfindings regarding recombination and differentiation in white-breasted nuthatches to examine abroad sampling of genomic differentiation in avian species pairs, to infer how chromosomelength (and thus rates of recombination) have shaped genome-wide patterns of differentiation.Through my research, I found that white-breasted nuthatches are comprised of fourdifferentiated populations that are on a continuum of differentiation and that ghost lineageintrogression has been involved in shaping these patterns. I also found evidence for largeinversion-like haploblocks occurring in white-breasted nuthatches. I then combined thesedifferentiation patterns with recombination estimates to show that broad-scale recombinationrates are negatively associated with differentiation. In my final chapter, I found that therelationship between differentiation and chromosome length varied among pairs, but thedirection of this relationship was significantly negatively correlated with the age of divergence.This result points to large chromosomes with lower rates of recombination being the likely areasto have higher amounts of differentiation in younger species.My dissertation spans a wide research scope, from species-specific questions to broadquestions about recombination and differentiation. It expands our knowledge of bird species bydescribing the genomic patterns of this cryptic species complex and how ghost lineageintrogression has provided important variation. My research also advances the field by adding tothe growing body of evidence that areas of low recombination are associated with regions ofincreased differentiation and that these landscapes of recombination likely shape genomicdifferentiation across bird species.

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Reproductive isolation among Sphyrapicus sapsuckers (2023)

The question “How and why do species split?” is the central motivation for this dissertation. Evolutionary biologists have long attributed this speciation process to barriers that interrupt gene flow, such as biological differences between populations that constrain gene exchange and cause isolation among formerly reproducing groups. However, more work is needed to answer what barriers are of key importance. Red-breasted, red-naped, and yellow-bellied sapsuckers are an excellent study system to understand the barriers that cause or maintain reduced gene flow because they are in the early stages of speciation. By studying both population dynamics in hybrid zones where different sapsuckers interbreed and genomic differentiation between species, I describe some of the barriers contributing to sapsucker isolation. In Chapter 2, I ask how the environment affects hybridization rates among sapsuckers. I use genomic data to demonstrate that red-breasted and red-naped sapsuckers hybridize to different extents in different environments, suggesting a strong effect of the environment on hybrid zone dynamics. Chapter 3 describes hybrid zone dynamics in an emergent tri-species hybrid zone. I show that all three species hybridize in one region in central British Columbia. However, they do not collapse into a hybrid swarm, so we propose this isolation is likely due to reduced fitness of hybrids. For Chapter 4 I examine how the level of differentiation between species varies across the genome and find that the Z chromosome shows much higher relative differentiation between species than the rest of the genome and harbors signatures of recurrent selection, high linkage disequilibrium, and likely results in epistasis among Z haplotypes. In Chapter 5, I ask what the genomic basis for sapsucker plumage is, as there are major changes in phenotype between sapsuckers, including a shift from sexually monochromatic to dichromatic forms, which likely affect sapsucker mate choice and mating success. Genome-wide association tests indicate plumage is highly associated with the different Z haplotypes identified in Chapter 4. In summary, within this dissertation I present evidence that post-zygotic isolation likely reduces hybrid fitness via both extrinsic (environmental) and intrinsic (genetic incompatibility) means.

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Genomic architecture of speciation in a warbler species complex (2020)

My PhD research investigated the mechanism of speciation in natural populations. Despite a great progress made since the ‘modern synthesis’ on the genetic basis of speciation, no consensus has been reached in terms of the genomic architecture of speciation: whether speciation is initiated by many regions (scattered across the genome), each of small effects on traits under weak selection (divergent selection or reinforcement), or a few regions that have strong effects on traits under strong selection. Understanding the genomic architecture of speciation is important because it determines whether reproductive isolation could effectively evolve when the diverging lineages still hybridize. I investigated this question in a Setophaga warbler species pair at the early stage of divergence: Townsend’s (Setophaga townsendi) and Hermit warblers (S. occidentalis). These two species hybridize extensively in the hybrid zone in Washington Cascades, demonstrating stable genomic clines over decades. This species complex demonstrates clear pattern of ‘selection with gene flow’, in which a few regions of large effects under strong divergent selection are highly differentiated between lineages, although the rest of the genomes are homogenized by gene flow. These nuclear genomic regions under selection are related to plumage coloration and mitochondrial fatty acid metabolism and are tightly associated with climatic variation among sites. Altogether, mitonuclear adaptation and selection on pigment patterning are prevailing evolutionary forces that counteract gene flow and allow speciation in this warbler system to proceed, despite ancient admixture and ongoing hybridization.

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Migratory divides and the genetic basis of reproductive isolation (2015)

Differences in seasonal migratory behaviour could be an important driver of ecological speciation. Many divergent groups form migratory divides on their breeding grounds; they breed adjacent to one another but use different routes to navigate around unsuitable areas on migration. Hybrids in divides are predicted to employ intermediate and inferior routes. I used light-level geolocators to track birds from the edges and center of a hybrid zone between inland and coastal Swainson’s thrushes (Catharus ustulatus) in western Canada. These data provided the first direct identification of a migratory divide (Chapter 2) and support for the prediction that hybrids in divides take intermediate routes (Chapter 3). Hybrid routes crossed arid and mountainous regions, further suggesting that these routes are inferior.I extended this work to examine the genetic basis of reproductive isolation between thrushes, assembling a reference genome and generating whole-genome sequence data for populations adjacent to the hybrid zone between these groups (Chapter 4). I documented genome-wide heterogeneity in genetic differentiation and uncovered patterns suggesting selective sweeps and variation in recombination generated this heterogeneity; within-population variation and absolute genetic differentiation were lower in regions of high relative differentiation and these reductions often coincided with centromeres and the Z chromosome. Genes associated with migration were concentrated in highly differentiated areas, further supporting migration’s role in reproductive isolation between thrushes.I complimented this work using a comparative approach to determine if patterns in the Swainson’s thrush could be extended to other species (Chapter 5). Specifically, I compared rates of phenotypic divergence between sister pairs that form divides and those that do not. I considered phenotypic divergence a proxy for reproductive isolation and contrary to expectations, found divergence was greater among taxa that do not form divides. This pattern could be explained by differential fusion, with sister pairs that do not form divides fusing into a single unit during periods of secondary contact unless they were sufficiently diverged phenotypically. Differences in migration would have permitted the persistence of pairs that form divides even without phenotypic differentiation. Under this scenario, migration serves as one of the major sources of speciation in North American birds.

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Hybridization, Speciation and the Biogeography of Genetic and Phenotypic Variation in Setophaga Warblers (2014)

Contact zones between previously isolated taxa provide natural systems for studying the processes involved in divergence, adaptation and reproductive isolation. In this thesis I use inferences drawn from biogeographic patterns and the characteristics of hybrids to understand the evolutionary processes involved in the production and maintenance of avian contact zones. In chapter two, I use genetic and phenotypic data from two related species of wood warbler to study the hybridization dynamics between them. I found that Setophaga virens and S. townsendi hybridize extensively where they come into contact but that the hybrid zone between them is narrow, suggesting moderate selection against hybrids. In chapter three and four I examine a possible mechanism of selection within such hybrid zones: differences in seasonal migratory behaviour. I explore this in a hybrid zone between S. coronata and S. auduboni. In chapter three I use isotopic data from breeding birds to make inferences about the wintering behaviour of hybrids. In chapter four, I use genetic data and video-based orientation assays of birds on fall migration to estimate the migratory tendency of birds in the hybrid zone. I found that (1) isotopes suggest that birds in the hybrid zone mostly wintered in the southeastern U.S. and (2) birds, on average, oriented towards the northeast during fall migration, regardless of their genetic background.These hybrid zones illustrate patterns of concordance between some characteristics but discordance in others. As I review in chapter five, the biogeographic patterns associated with discordant molecular markers, especially between those in the nuclear versus mitochondrial genome, can reveal novel insights into important evolutionary processes. In chapter six I address an example of such discordance, where previous research has suggested that mitochondria from S. coronata have introgressed throughout much of the range of S. auduboni. I use genetic, biochemical, and phenotypic variation to show that this shift in mitochondria is correlated with a shift in migratory behaviour and with some aspects of mitochondrial phenotype. In chapter seven, I use a genome-wide assay of tens of thousands of nuclear polymorphisms to test whether mtDNA is truly an outlier as compared to the nuclear genome.

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Understanding parapatric range limits in the long-toed salamander, Ambystoma macrodactylum (2014)

Understanding geographic range limits is an outstanding challenge in evolutionary ecology. My goal was to characterize and evaluate factors contributing to parapatric borders in the long-toed salamander (Ambystoma macrodactylum). Using amplified fragment length polymorphism and mitochondrial data, I tested whether currently-recognized subspecies of long-toed salamander are distinct evolutionary units. My results demonstrate that the long-toed salamander consists of at least four divergent lineages. Discordance between these lineages and current subspecies designations, as well as evidence for a cryptic lineage, emphasize the need to reevaluate existing taxonomy prior to conducting studies of species’ range limits. To further understand the distribution of diversity in this system, I explored the role of climate in shaping lineage boundaries. Using spatial data and ecological niche modeling, I asked whether the boundaries between lineages reflect the limits of their respective climatic niches. My results suggest that the different long-toed salamander lineages are ecologically similar and that suitable climatic space for each lineage exists well-beyond shared borders. Although some contact zones coincide with areas where the average climatic suitability for both lineages is low, sites that are highly suitable for each lineage can be found within these regions in all cases. Thus climatic barriers alone are unlikely driving range limits in this system. I next examined the role of hybridization in shaping range limits. I characterized fine-scale patterns of genetic structure in a contact zone between two long-toed salamander lineages. To determine whether there is evidence of hybrid dysfunction, I assayed adult feeding performance in the laboratory. I observed reduced feeding performance in populations coinciding with the extent of mitochondrial introgression but not in populations that are more admixed. These results may be relevant for understanding the limits of introgression for some genes, but not all. Thus the study of range limits in the context of hybrid zones may require consideration of factors governing differential rates of introgression across the genome. This dissertation demonstrates the use of multiple lines of investigation to narrow down the most relevant hypotheses for parapatric range limits and highlights the potential for several factors to ultimately be shaping species’ range limits.

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Hybridization and speciation in the Yellow-rumped Warbler complex (2010)

No abstract available.

Master's Student Supervision

Theses completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest theses.

Patterns of genomic differentiation and hybridization between two merging Emberizidae species implicate a sex chromosome inversion in plumage variation (2021)

Hybrid zones offer researchers the opportunity to investigate how evolutionary processes interact to drive speciation forward. However, in these areas where genetic divergence competes against gene flow, speciation and population merging are both possible with the outcome dependent on the strength of reproductive barriers between groups. The yellowhammer (Emberiza citrinella) and pine bunting (Emberiza leucocephalos) are Palearctic songbirds with highly divergent plumage patterns. Despite their differences, these taxa hybridize extensively and show negligible differentiation in their mitochondrial genomes. These observations create a conflicting picture of the state of reproductive barriers between groups, raising the question whether yellowhammers and pine buntings are actually separate species. In this thesis, I examine patterns of genetic variation among phenotypically pure and hybrid individuals to assess the strength of reproductive isolation between taxa. I hypothesize that, unlike mitochondrial differentiation, nuclear differentiation will be moderate and that patterns of divergence will reflect some weak reproductive isolation between groups. I find that, in allopatry, yellowhammers and pine buntings separate into distinct genetic clusters based on an island of differentiation on the Z chromosome. Yet, in other parts of the genome, I find evidence of past mitonuclear gene introgression. In sympatry, I report a breakdown of allopatric genetic clusters driven by extensive interbreeding. These findings combined with the high number of late generation hybrids identified within the sympatric zone suggest that reproductive barriers are weak between taxa. Interestingly, I further find low recombination within the island of differentiation identified between allopatric populations implying that this region may house a chromosomal inversion. The inversion is highly associated with plumage variation and may be responsible for the maintenance of parental phenotypes within the sympatric zone. Because reproductive barriers are weak, it is likely that hybridization will continue between yellowhammers and pine buntings potentially leading to the merging of these groups, but that the putative inversion could preserve parental plumage phenotypes within this single species. Retention of such variation would increase the evolvability of the system such that the population could be safeguarded from extinction or, if evolutionary pressures change, could diverge again and move towards speciation.

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Geographic variation in song and genetics in the Townsend's Warbler (Setophaga townsendi) (2019)

Bird song is shaped by both genetic and cultural processes, presenting a particularly tractable system for understanding the connection between communication and reproductive barriers that drive diversification. Song dialects—or differences in song structure across geographic space—can act as signposts of cultural differences between populations, which may also indicate genetic differences in the population. The Townsend’s Warbler (Setophaga townsendi) is a species with geographic variation in mitochondrial genetic signatures. I investigate if concurrent variation occurs in song and nuclear genetic signatures, by describing the geographic variation of song and nuclear DNA across Townsend’s Warbler range. I quantify distinct song types and patterns across Townsend’s Warbler populations, along with patterns of genetic variation across their range using genotype-by-sequencing data. If genetic and cultural processes are tightly linked, I expect song to vary between regions of genomic differentiation. I demonstrate that individuals have a repertoire of at least two distinct song types—consistent with the two-song-type pattern common in Parulid warblers—but find this pattern is less evident in a range-wide comparison. There is extensive variability in Type I song, whereas Type II song is more stereotyped across the range. There is little distinct grouping that coincides between song and the isolation-by-distance pattern in the nuclear DNA. A mismatch between song and genetic patterns suggests that song divergence is not predicted solely by genotype. By characterizing the within-species variation in song and genetic structure, we can expand our understanding of the dynamic interplay between cultural traits and population structuring.

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Genomic differentiation of Northern Goshawks in coastal British Columbia (2018)

Understanding the process by which populations become genetically differentiated from one another has been a central goal of population genetics since its inception. With the loss of biodiversity across the globe, we lose information regarding how populations of organisms separate and become genetically distinct. An organism that exemplifies this issue is a subspecies of the Northern Goshawk (Accipiter gentilis laingi; hereafter simple “laingi”) which is classified as Threatened in coastal British Columbia under the Species at Risk Act (Canada) and the Endangered Species Act (USA). Using genotyping-by-sequencing (GBS) data across thousands of SNPs (single nucleotide polymorphisms), we investigate the genetic differentiation of this subspecies and infer the processes governing its distinctiveness. We find that Northern Goshawks on the archipelago of Haida Gwaii are distinct from other populations, clearly separating in principal component analyses, and have a wider distribution of FST and DXY when compared to other populations. In other populations, we recovered weak differentiation ranging from coastal BC to Maine; these populations likely represent the other North American subspecies Accipiter gentilis atricapillus (hereafter, simply “atricapillus”). The second phase of our research was to clarify the range of the laingi subspecies, which previously had been under debate. By selecting laingi-informative single nucleotide polymorphisms (SNPs) from our sequencing data we were able to develop SNP genotyping assays that allowed for the inclusion of hundreds of additional low-quality samples. Using these assays, we find that laingi goshawks are largely restricted to Haida Gwaii. Additionally, we wanted to understand the processes driving differentiation in Haida Gwaii and gene flow between other populations and Haida Gwaii. We found that even though Haida Gwaii is a small population, strong selection is likely shaping the genome. By jointly analyzing our GBS and genotyping data we find that gene flow between Haida Gwaii and other populations is likely low. This thesis contributes to knowledge of a Threatened bird of prey and more generally to how evolutionary distinctness evolves in geographically separated populations of organisms.

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Factors affecting the efficacy of biodiversity conservation in tropical protected areas: a case study in Xishuangbanna, southwestern China (2017)

Protected areas have long been considered the backbone of biodiversity conservation strategies. However, whether protected areas are truly effective at conserving biodiversity remains an important question. Factors affecting the efficacy of biodiversity conservation in protected area are complex - human population density, policy enforcement, and local community attitudes towards conservation could all influence conservation outcomes. In this study, I measured how attitudes towards conservation and perception of law enforcement (based on 354 questionnaire surveys) in communities surrounding protected areas was associated with wildlife within the protected areas. I used motion-triggered camera traps (12,148 camera-trap days in total) and Bayesian hierarchical statistical models to estimate occupancy rates for four commonly hunted mammal species, as well as the species richness of medium- to large-sized mammals in six protected areas in Xishuangbanna, southern China, a diverse sub-tropical region with high hunting and land conversion pressures. I found that abundance of the large size species-wild boar (Sus scrofa) and small size Asian palm civet (Paradoxurus hermaphroditus), was positively correlated with park size. However, the villager-reported number of punishments the park meted out for law violations, and the villager-reported frequency of outreach by park staff to the local communities did not have significant effects on population size as well as richness of wildlife. Mammal diversity of mammal across parks was more correlated with villager-reported law enforcement effort than with outreach, even in parks surrounded by large human populations. My study highlighted the importance of reserve size, adequate habitat is the key of maintaining wildlife population in this area. My study provides insights that protected areas that have stricter enforcement as well as more frequent outreach activities could be more effective and our approach is applicable to assess effects of conservation actions on wildlife.

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An analysis of ecological traits as reproductive barriers between the MacGillivray's (Geothlypis tolmiei) and Mourning (G. philadelphia) warblers (2015)

Speciation in birds is often thought to be influenced by ecological diversification, which may form barriers to reproduction between species. Ecological selection can act as a premating barrier by reducing the chance of interactions between species, or as a postmating barrier if hybrids have ecological traits that are unfavourable. My objective in this study is to understand the role of ecological traits in maintaining isolation between MacGillivray’s (Geothlypis tolmiei) and Mourning warblers (G. philadelphia), which are two songbird species that form a narrow hybrid zone in northeastern British Columbia. I generate ecological niche models for each species to investigate whether the niche might have a role in explaining the location and width of the hybrid zone by comparing niche and range limits, and whether there is evidence for niche divergence. I show that the species have niches that are similar but have diverged in climatic variability and precipitation measures. These differences may partly explain why the niche models predicted that geographic regions within a species’ own range were the most suitable for that species. The contact zone was the only region where both models predicted high suitability, suggesting that hybridization occurs only where conditions are suitable for both species. I also present two analyses of how genotype is related to ecological characteristics in the hybrid zone. I use the niche models to predict the relative suitability of locations where birds occupied breeding territories in the hybrid zone and compared the relative scores among a gradient of hybrid genotypes. At those same hybrid zone territories I measure microhabitat characteristics of territories and conducted a Principal Component Analysis to examine whether there is a relationship between microhabitat of territories with genotype. I found no evidence that genotype was related with ecological traits in the hybrid zone. This suggests that when under the same ecological conditions the two species are ecologically equivalent, and that hybrids likely do not experience a disadvantage in terms of the ecological traits of their breeding territories. Overall, these results suggest that niche divergence likely had only a small role in the diversification between the MacGillivray`s and Mourning warblers.

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Song in a hybrid zone between Townsend's (Setophaga townsendi) and black-throated (S. virens) warblers (2014)

Song is one of the most widely recognized premating barriers to reproduction between avian species. In oscines both genetic and cultural inheritance contribute to an individual’s song phenotype, contributing to difficulty in predicting the role that song may play in reproductive isolation; interspecific song learning could promote interbreeding. Here I seek to better understand this phenomenon by studying song in a narrow hybrid zone between black-throated green (Setophaga virens) and Townsend’s warblers (S. townsendi). I use multivariate analyses to compare songs in the hybrid zone to those found in allopatry, predicting that if song is a strong barrier to interbreeding, then there should be a relationship between song and genotype in the hybrid zone. I employ a genotyping-by-sequencing (GBS) method to identify thousands of markers and develop two hybrid indices. Playback experiments were carried out in the field to test responses to parental songs, and a cline analysis was conducted in order to compare transitions in genotype and song across the hybrid zone. I show that only parental song types are found in the hybrid zone, and furthermore, that there is little if any association between song and genotype in sympatric individuals; this suggests that song is not an important reproductive barrier. Allopatric individuals responded only to local songs, indicating that individuals may exhibit a learned response to songs that they are commonly exposed to. Out of thousands of genomic markers, I identified few that were diagnostic, suggesting that much of the genome may introgress freely between these species. I observed discordance between the song and genotype clines; the song cline was much narrower indicating that song is under stronger selection. Taken together, these findings combine to suggest that song is not a reproductive barrier in this hybrid zone, but is instead a cultural trait that is maintained by frequency-dependent selection. Thus, it may be more beneficial for males to sing a locally common song than to broadcast accurate species-membership information.

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