Dolph Schluter

Professor

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Graduate Student Supervision

Doctoral Student Supervision (Jan 2008 - Mar 2019)
Detecting the drivers of divergence : identifying and estimating natural selection in threespine stickleback (2016)

Differences in ecological factors between habitats drive evolutionary divergence and can lead to the generation of new species. While many studies provide evidence suggesting a given trait or genetic locus is adaptive few studies are able to elucidate the direct mechanisms responsible for differences in fitness. I use experimental and observational studies in threespine stickleback (Gasterosteus aculeatus) to identify factors that have driven divergence and to disentangle the mechanisms by which differential fitness arises.To disentangle direct selection on a phenotype from selection on correlated characters encoded by its underlying gene, I applied statistical methods for the estimation of selection on correlated characters (Chapter 2). These data provided the first evidence of direct selection on the lateral plate phenotype and suggested that pleiotropy at the Ectodysplasin locus is likely an important factor driving the rapid and repeated evolution of armour phenotypes.Spectral sensitivity is thought to evolve to match features of the local light environment. Marine and freshwater threespine stickleback inhabit divergent light environments and therefore provide an opportunity to test the hypothesis of spectral matching. I surveyed the opsin gene expression and spectral sensitivity of multiple marine and freshwater populations to test this hypothesis (Chapter 3). While I find weak evidence for spectral matching, I do find evidence suggesting adaptive divergence of spectral sensitivity between populations inhabiting different light environments.Competition is widely appreciated to play a direct role in driving trait divergence; however, it can also have indirect effects mediated through differential exposure to predators. To test for the contribution of species interactions to phenotypic and genetic divergence I conducted an experiment that manipulated exposure of threespine stickleback to a predator, coastaliicutthroat trout (Chapter 4). After one generation of differential exposure to trout there was evidence of phenotypic and genetic divergence between treatments. These results suggest that cutthroat trout are an important source of divergent selection between populations of threespine stickleback.These studies suggest that bony armour and visual sensitivity are locally adapted and that pleiotropy and genetic architecture likely play an important role in determining evolutionary trajectory during the adaptation of threespine stickleback to freshwater habitats.

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Intraguild predation is a mechanism of divergent selection in the threespine stickleback (2016)

Biotic interactions among species are thought to be important for the generation of phenotypic diversity. Intraguild predation is a common ecological interaction that occurs when a species preys upon another species with which it competes. This interaction is potentially a mechanism of divergence between intraguild prey populations, but it is unknown if cases of character shifts in intraguild prey are phenotypically plastic or an evolutionary response. I collected threespine stickleback (Gasterosteus aculeatus) from lakes with and without prickly sculpin (Cottus asper) and identified trait differences in armour and behaviour among populations in the wild. Differences in behavioural and morphological traits among freshwater populations persisted in a common garden, suggesting that adaptation to intraguild predation has a genetic basis. To date, the evolutionary effect that biotic selection has upon an organisms’ genome remains largely unknown in natural populations. I used whole genome re-sequencing to investigate the extent of genetic differentiation between stickleback from populations with and without sculpin. The main axis of genetic variation in these populations is strongly associated with the presence or absence of sculpin. I identified the regions of the genome that have differentiated in parallel between lakes with and without sculpin, and measured the strength of this divergence. The presence or absence of sculpin corresponds to widespread differentiation that is unevenly distributed across the stickleback genome. Adaptation to intraguild predation may involve hundreds of genes with diverse functions. Observations of extensive phenotypic and genetic differentiation between stickleback from lakes with and without sculpin provide indirect evidence that sculpin are the cause of trait differences. Pelvic morphology is one of the most conspicuously varying traits among freshwater stickleback populations. This variation has been hypothesized to be the result of predation by fish and/or insect predators. I conducted a selection experiment to test if sculpin were an agent of selection for pelvic spine length. The results were combined with other experimental selection studies and used in a meta-analysis. Fish predators are an agent of selection for longer pelvic spines, but the role of insect predators is still unclear. Intraguild predation is a mechanism of divergent selection in threespine stickleback.

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The ecological consequences of evolutionary change in freshwater ecosystems (2016)

Evolutionary change has largely been ignored in ecology because it has traditionally been considered too gradual a process to alter ecological patterns. Recent evidence that evolution can occur rapidly has challenged this notion. Understanding when evolution is likely to alter ecological processes and how evolution changes ecological dynamics could improve our understanding of community and ecosystem ecology and lead to greater predictability. In chapter 2 I present the results of an experiment investigating how local adaptation in two species alters community structure and ecosystem function. I found that intraspecific variation between these two taxa can interact to alter both the ecological community and some ecosystem functions. In chapter 3 I focus on understanding how rapid evolution from introgressive hybridization alters ecology in both a mesocosm experiment and a comparative field study. I found that introgressive hybridization lead to a phenotypic shift and predictable changes in community structure and ecosystem function based on trophic cascade theory. In chapter 4 I detail the findings from a large-scale piscivorous fish trophic cascade experiment. In this study I found that the addition of a piscivore alters the movement of invertebrates from aquatic environments to terrestrial environments. In addition, the results support previous findings that non-consumptive effects of predators may play an important role in determining the strength of the trophic cascade in the aquatic system. In chapter 5 I explore the role of rapid evolution in enhancing and maintaining ecosystem services. I create a quantitative criteria for assessing the importance of rapid evolution to ecosystem services, review cases where rapid evolution may already be playing an important role, and suggest ways to manage for the conservation of ecosystem services.

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The evolutionary genomics of adaptation and speciation in the threespine stickleback (2016)

Speciation and adaptation are key processes in biological evolution. Speciation creates genealogically discrete lineages, whereas adaptation causes organisms to become better matched to their environments. In this thesis, I conducted three studies that advanced our knowledge of speciation or adaptation. All three studies made use of a unique study system: threespine stickleback – small fish found in marine and fresh waters throughout the northern hemisphere. I first explored the potential of a newly-discovered “white” form of threespine stickleback for studying the early phases of speciation. Using a variety of population genomic methods, I showed that white stickleback are genetically distinct from other marine stickleback, and diverged recently in the face of substantial gene flow. These features make white stickleback an excellent system for studying the early phases of speciation. Next, I used white stickleback to examine the role of sexual and trophic divergence in the early phases of speciation. Using morphological and isotopic data, I found evidence for only weak trophic differentiation between white and common stickleback. Instead, genetic differences between the two forms are concentrated on genomic regions that harbour genes with male-biased expression. This suggests that, apart from difference in body size, strong trophic differentiation may not be necessary in the early phases of speciation. The final study explored the role of gene flow in shaping the genomic architecture of adaptation. Theory predicts that when adaptation occurs in the face of gene flow, genomic architectures in which adaptive loci are localized in regions of low recombination will be favored over others. I tested this prediction by quantifying the correlation between recombination rate and the density of adaptive loci in pairs of stickleback populations that varied in their degree of gene flow. In line with theory, we found that adaptive loci were more like to be found in regions of low recombination when divergent selection and gene flow co-occurred. Together, the studies presented in this thesis provide new tools and significant advances in our understanding of speciation and adaptation.

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The genetics of adaptation and speciation in threespine stickleback species pairs (Gasterosteus aculeatus species complex) (2014)

Ecological speciation appears to be a common process by which new species arise and the genetics underlying the process can substantially affect its outcome. Replicate ‘benthic and limnetic’ pairs of threespine stickleback species are an ideal system with which to study the genetics underlying ecological speciation. My first question was: what genetic mechanisms link divergent natural selection to reproductive isolation during ecological speciation? In chapter 2, I present an experiment designed to determine what genetic mechanism links divergent selection on body size to assortative mating by body size in the Paxton Lake species pair. I found that body size functions as a mate signal trait and determines female mate preference via phenotype matching. This implies that genes under divergent selection are the same as those underlying both components of assortative mating, a mechanism that should facilitate ecological speciation with gene flow. My second question was: what is the genetic architecture of adaptation during ecological speciation? In chapter 4, I used QTL mapping to discover the genetic architecture underlying a large number of parallel morphological differences in the Paxton and Priest Lake species pairs and found it to be polygenic and widespread throughout the genome in both. This suggests that many loci underlying ecologically important traits have diverged (and/or divergence has persisted) during ecological speciation despite homogenizing gene flow. My third question was: how predictable are the genetics of adaptation during ecological speciation and in general? Chapters 3 and 4 describe the first studies to quantitatively address this question. In chapter 4, I found that about 50% of QTL for parallel morphological differences are parallel in the two species pairs. Also, on average, the proportional similarity of QTL use underlying individual traits is about 0.4. In Chapter 3, I present the results of a meta-analysis of the genetics underlying repeated phenotypic evolution in natural populations. Using an impartial literature review, I found that the average probability of gene reuse was 0.32 - 0.55. I also found that the probability of gene reuse declined with increasing age of the taxa compared.

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Evolution of the trophic niche and food web structure (2011)

Food webs – networks of predator-prey interactions – are of fundamental importance to the ecological and evolutionary dynamics of biodiversity. The stability and functioning of food webs can be dependent on their 'vertical' structure: the distribution of species' trophic positions, the length of food chains and the prevalence of omnivory. Food web interactions such as predation, resource competition and intraguild predation can be potent agents of natural selection, driving evolutionary responses that feed back to reconfigure the food web. The structure and function of food webs thus arises from an interplay of ecological and evolutionary processes.My thesis describes four studies of the evolutionary ecology of food webs. First, I test whether trophic position evolution is associated with speciation events in Sebastes rockfish. My phylogenetic comparative analyses find no signal of change at speciation in the evolution of trophic position or trophic morphology. Instead, speciation events in rockfish appear to be primarily associated with divergence in depth habitat in the ocean.Next, I use an evolutionary assembly model to explore how the strength of foraging trade-offs influences the structure and temporal dynamics of food webs, as well as patterns of trait evolution. Across a range of trade-off strengths, the amount of omnivory in a food web is positively related to both species turnover and the degree of convergence in trophic position evolution. I then fit macroevolutionary models to Sebastes trophic position data. The data support a model of recurrent evolution in a constrained trait space, as predicted for omnivorous consumers.Finally, I examine the ecological and evolutionary consequences of intraguild predation on three spine stickleback (Gasterosteus aculeatus) by prickly sculpin (Cottus asper). My collaborators and I use comparative and experimental studies to show that sculpin presence in lakes is associated with the evolution of antipredator and pelagic foraging morphology in stickleback, leading to reduced predator vulnerability, increased zooplanktivory, and changes to the structure of the food web.These studies address a number of important questions about how evolutionary processes influence food web structure and function, and illustrate the work that remains to be done in this exciting area of research.

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The genetics of adaptation in stickleback (2010)

No abstract available.

Mechanisms of Divergence in Threespine Stickleback (Gasterosteus Aculeatus) (2009)

No abstract available.

Master's Student Supervision (2010-2017)
Components of premating reproductive isolation in threespine stickleback (2011)

Reproductive isolation, the reduction in gene flow between two species, is central to the study of speciation. Many so-called isolating barriers may be involved in preventing two species from successfully hybridizing, but the importance of each barrier and the presence of interactions between them have not often been measured. I investigated habitat and mating isolation in the recently diverged benthic-limnetic species pairs of threespine stickleback (Gasterosteus aculeatus species complex). In these species, the males of which build nests and guard territories during the breeding season, there is a strong pattern of male habitat choice, with limnetics nesting in open habitats and benthics nesting under vegetation. When males were given a choice of nesting habitats in enclosures in an artificial pond, they almost always chose according to this pattern. However, females displayed no difference in probability of spawning with conspecifics in different habitats in no-choice mating trials, making habitat isolation at best a weak barrier to hybridization in the absence of interactions with other isolating mechanisms. From an existing dataset of mate choice trials, I calculated the contributions of body size differences and male nuptial colour to mating isolation. Isolation due to body size differences was strong in both species, but stronger in benthics. Isolation due to colour preference was negligible in benthics and moderately strong in limnetics. Generalized linear models indicated that interactions with other, unspecified species-specific traits increases isolation due to body size and, in benthics, due to colour. Together, these traits provide strong but incomplete premating isolation, resulting in an expected hybridization rate higher than that observed in nature, and thus are not sufficient in themselves to maintain the species pairs.

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Adaptive significance of pelvic girdle loss in threespine stickleback (2010)

Pelvic girdle loss has evolved repeatedly in freshwater stickleback. In many casesit is caused by a mutation in a regulatory sequence that controls expression of themajor pelvic girdle locus (Pitx1) in the prospective pelvic region. Pelvic girdleloss can spread rapidly through populations, but its adaptive significance is not wellunderstood. I experimentally tested potential ecological mechanisms for pelvic girdle loss in juvenile threespine stickleback. I carried out two insect predation experiments to measure selection on pelvic spine length and body size, and to measure the effect of the pelvic girdle on survival. In the first experiment, the pelvic spines of all fish were clipped to varying degrees to artificially create variation in spine length. For the second experiment, I created hybrid backcross families, where 50% of the offspring expressed pelvic girdle loss. In both experiments, the fish were exposed to predation by a common aquatic insect predator. Selection tended to favour shorter spines, increased body size and loss of the pelvic girdle. A third experiment measured growth rates in juvenile fish with and without a pelvic girdle, to test for a potential growth rate advantage of the "without" phenotype. On average, "withouts" exhibited a nonsignificant trend for higher growth rates compared to "withs".As the power of the predation experiments was low, I performed meta-analyses to combine my data with previously published experiments. Across these experiments, insect predators selected for shorter pelvic spine length as well as increased body size. There was no mean positive or negative effect of the pelvic girdle on survival in the face of insect predation, but the confidence interval for this result was wide, and further studies are required.My findings suggest that predation may drive pelvic girdle loss in juvenile stickleback by means of selection against correlated traits, such as long pelvic spines, rather than selection against the pelvic girdle itself. I did not detect any significant association between pelvic girdle loss and increased growth rates. It thus remains undetermined if selection for increased body size acts as an additional selection factor for pelvic girdle loss.

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