Darren Irwin

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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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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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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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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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 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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No abstract available.