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Graduate Student Supervision
Doctoral Student Supervision (Jan 2008 - May 2021)
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.
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.
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.
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.
No abstract available.
Master's Student Supervision (2010 - 2020)
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.
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.
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.
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.
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.
Recent Tri-Agency Grants
The following is a selection of grants for which the faculty member was principal investigator or co-investigator. Currently, the list only covers Canadian Tri-Agency grants from years 2013/14-2016/17 and excludes grants from any other agencies.
- Comparative genomic analysis of hybridization and speciation: uncovering genes and traits responsible for diversification - Natural Sciences and Engineering Research Council of Canada (NSERC) - Discovery Grants Program - Individual (2013/2014)
- Hybridization and the coexistence of species (2021)
- Mitonuclear co-introgression opposes genetic differentiation between phenotypically divergent songbirds (2021)
- Ongoing production of low-fitness hybrids limits range overlap between divergent cryptic species (2021)
- Ongoing production of low‐fitness hybrids limits range overlap between divergent cryptic species (2021)
- Signatures of mitonuclear coevolution in a warbler species complex (2021)
Nature Communications, 12 (1)
- Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species (2020)
- Assortative mating in hybrid zones is remarkably ineffective in promoting speciation (2019)
- Population genomic analyses reveal a highly differentiated and endangered genetic cluster of northern goshawks ( Accipiter gentilis laingi ) in Haida Gwaii (2019)
Evolutionary Applications, 12 (4), 757--772
- A comparison of genomic islands of differentiation across three young avian species pairs (2018)
Molecular Ecology, 27 (23), 4839--4855
- Population genomic analyses reveal a highly differentiated genetic cluster of northern goshawks (Accipiter gentilis laingi) in Haida Gwaii (2018)
- Sex chromosomes and speciation in birds and other ZW systems (2018)
- Cultural isolation is greater than genetic isolation across an avian hybrid zone (2017)
Journal of Evolutionary Biology, 30 (1), 81-95
- First Record of House Swift (Apus nipalensis) in the Americas (2017)
Wilson Journal of Ornithology, 129 (2), 411-416
- Linking the wintering and breeding grounds of warblers along the Pacific Flyway (2017)
Ecology and Evolution, 7 (17), 6649-6658
- Migratory orientation in a narrow avian hybrid zone (2017)
- A tree of tree frogs around the Black Sea (2016)
Molecular Ecology, 25 (17), 4093-4096
- Genomic approaches to understanding population divergence and speciation in birds (2016)
Auk, 133 (1), 13-30
- Genomic variation across the Yellow-rumped Warbler species complex (2016)
Auk, 133 (4), 698-717
- Low levels of hybridization across two contact zones among three species of woodpeckers (Sphyrapicus sapsuckers) (2016)
Journal of Avian Biology, 47 (6), 887-898
- Phenotypic and genetic analysis support distinct species status of the Red-backed Woodpecker (Lesser Sri Lanka Flameback: Dinopium psarodes) of Sri Lanka (2016)
Auk, 133 (3), 497-511
- Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in a ring species (2016)
Molecular Ecology, 25 (18), 4488-4507
- Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in greenish warblers (2016)
- Strong reproductive isolation and narrow genomic tracts of differentiation among three woodpecker species in secondary contact (2016)
Molecular Ecology, 25 (17), 4247-4266
- The Genetics of Seasonal Migration and Plumage Color (2016)
Current Biology, 26 (16), 2167-2173
- Conflicting effects of microhabitats on Long-toed Salamander (Ambystoma macrodactylum) movement: implications for landscape connectivity (2015)
Canadian Journal of Zoology, 93 (1), 1-7
- Genomic analysis of a migratory divide reveals candidate genes for migration and implicates selective sweeps in generating islands of differentiation (2015)
Molecular Ecology, 24 (8), 1873-1888
- Phenotypic divergence during speciation is inversely associated with differences in seasonal migration (2015)
Proceedings of the Royal Society B-Biological Sciences, 282 (1819)
- The importance (or lack thereof) of niche divergence to the maintenance of a northern species complex: the case of the long-toed salamander (Ambystoma macrodactylum Baird) (2015)
Journal of Evolutionary Biology, 28 (4), 917-930
- A call for the preservation of images, recordings, and other data in association with avian genetic samples, and the introduction of a solution: OMBIRDS (2014)
Auk, 131 (3), 321-326
- Genomic divergence in a ring species complex (2014)
Nature, 511 (7507), 83-U433
- Hybrid songbirds employ intermediate routes in a migratory divide (2014)
Ecology Letters, 17 (10), 1211-1218
- Individual performance in relation to cytonuclear discordance in a northern contact zone between long-toed salamander (Ambystoma macrodactylum) lineages (2014)
Molecular Ecology, 23 (18), 4590-4602
- Isotopic variation across the Audubon's-myrtle warbler hybrid zone (2014)
Journal of Evolutionary Biology, 27 (6), 1179-1191
- MIGRATION, MITOCHONDRIA, AND THE YELLOW-RUMPED WARBLER (2014)
Evolution, 68 (1), 241-255
- DIFFERENTIAL MIGRATORY TIMING OF WESTERN POPULATIONS OF WILSON'S WARBLER (CARDELLINA PUSILLA) REVEALED BY MITOCHONDRIAL DNA AND STABLE ISOTOPES (2013)
Auk, 130 (4), 689-698
- A novel approach for finding ring species: look for barriers rather than rings (2012)
Bmc Biology, 10
- A robust new metric of phenotypic distance to estimate and compare multiple trait differences among populations (2012)
Current Zoology, 58 (3), 426-439
- Concordance of genetic and phenotypic characters across a sapsucker hybrid zone (2012)
Journal of Avian Biology, 43 (2), 119-130
- Culture in Songbirds and Its Contribution to the Evolution of New Species (2012)
Creating Consilience: Integrating the Sciences and the Humanities,
- Dramatic intraspecific differences in migratory routes, stopover sites and wintering areas, revealed using light-level geolocators (2012)
Proceedings of the Royal Society B-Biological Sciences, 279 (1747), 4582-4589
- Large geographic range size reflects a patchwork of divergent lineages in the long-toed salamander (Ambystoma macrodactylum) (2012)
Journal of Evolutionary Biology, 25 (11), 2276-2287
- Local Adaptation along Smooth Ecological Gradients Causes Phylogeographic Breaks and Phenotypic Clustering (2012)
American Naturalist, 180 (1), 35-49
- CAN SONG DISCRIMINATE BETWEEN MACGILLIVRAY'S AND MOURNING WARBLERS IN A NARROW HYBRID ZONE? (2011)
Condor, 113 (3), 655-663
- Genetic variation and seasonal migratory connectivity in Wilson's warblers (Wilsonia pusilla): species-level differences in nuclear DNA between western and eastern populations (2011)
Molecular Ecology, 20 (15), 3102-3115
- Hybrid origin of Audubon's warbler (2011)
Molecular Ecology, 20 (11), 2380-2389
- Hybridization between Townsend's Dendroica townsendi and black-throated green warblers D. virens in an avian suture zone (2011)
Journal of Avian Biology, 42 (5), 434-446
- MOLT, ORIENTATION, AND AVIAN SPECIATION (2011)
Auk, 128 (2), 419-425
- Who travels where: unraveling population structure, migratory connectivity, and song patterns in Western Sandpipers (2010)
Integrative and Comparative Biology, 50, E292
- Analysis of multilocus DNA reveals hybridization in a contact zone between Empidonax flycatchers (2009)
Journal of Avian Biology, 40 (6), 614-624
- Extensive hybridization in a contact zone between MacGillivray's warblers Oporornis tolmiei and mourning warblers O-philadelphia detected using molecular and morphological analyses (2009)
Journal of Avian Biology, 40 (5), 539-552
- Incipient ring speciation revealed by a migratory divide (2009)
Molecular Ecology, 18 (14), 2923-2925
- INCIPIENT SPECIATION DESPITE LITTLE ASSORTATIVE MATING: THE YELLOW-RUMPED WARBLER HYBRID ZONE (2009)
Evolution, 63 (12), 3050-3060
- Mitochondrial introgression and replacement between yellowhammers (Emberiza citrinella) and pine buntings (Emberiza leucocephalos) (Aves: Passeriformes) (2009)
Biological Journal of the Linnean Society, 98 (2), 422-438
- Speciation: New Migratory Direction Provides Route toward Divergence (2009)
Current Biology, 19 (24), R1111-R1113
- Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): a strong role for stochasticity in signal evolution? (2008)
Journal of Evolutionary Biology, 21 (2), 435-448
- Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses (2008)
Molecular Ecology, 17 (11), 2691-2705
- Green Warbler Phylloscopus (trochiloides) nitidus recorded at Ottenby, Öland: A first record for Scandinavia (2007)
Ornis Svecica, 17 (2), 75-80
- Conflicting patterns of mitochondrial and nuclear DNA diversity in Phylloscopus warblers (2006)
Molecular Ecology, 15 (1), 161-171
- Speciation by distance in a ring species (2005)
Science, 307 (5708), 414-416
- The role of phenotypic plasticity in driving genetic evolution (2003)
Proceedings of the Royal Society of London Series B-Biological Sciences, 270 (1523), 1433-1440
- Blowfly Trypocalliphora braueri (Diptera: Calliphoridae) larvae infestation in Willow Warblers Phylloscopus trochilus breeding in a hybrid zone (2002)
Ornis Svecica, 12 (1), 83-88
- Circular overlaps: Rare demonstrations of speciation (2002)
Auk, 119 (3), 596-602
- Phylogeographic breaks without geographic barriers to gene flow (2002)
Evolution, 56 (12), 2383-2394
- The use of AFLP to find an informative SNP: genetic differences across a migratory divide in willow warblers (2002)
Molecular Ecology, 11 (11), 2359-2366
- Cryptic species in the genus Phylloscopus (Old World leaf warblers) (2001)
Ibis, 143 (2), 233-247
- Ring species as bridges between microevolution and speciation (2001)
Genetica, 112, 223-243
- Speciation in a ring (2001)
Nature, 409 (6818), 333-337
- Song variation in an avian ring species (2000)
Evolution, 54 (3), 998-1010
- Sexual imprinting, learning and speciation (1999)
Heredity, 82 (4), 347-354