Dolph Schluter

Competitive interactions among sympatric phenotypes shape forms of natural selection and evolution of phenotype distributions. Populations of fish in post-glacial lakes are a model system for studying the evolutionary outcomes of competition. Fish in these lakes tend to exhibit phenotypic variability corresponding to a nearshore (benthic/littoral) to open water (limnetic/pelagic) resource use axis. In several lakes, populations have repeatedly diversified into sets of sympatric ecotypes that are phenotypically distinct from each other. Competition is predicted to drive frequency-dependent selection within and among populations of post-glacial fish. We tested whether this form of selection acts within the range of phenotypes found in generalist, single-species populations of threespine stickleback. To do this, we used experimental mesocosms with differing frequency distributions of phenotypes. We found evidence for only weak frequency-dependent survival but not frequency-dependent growth. To evaluate evidence for a possible evolutionary outcome of competitive interactions, we tested the hypothesis that levels of ecological sexual dimorphism should be higher in populations that do not co-occur with competitor species. We found similar levels of sexual dimorphism in allopatric threespine stickleback populations compared to populations sympatric with another stickleback species or prickly sculpin (an intraguild predator). Instead, we found some evidence for an alternative hypothesis that sexual dimorphism might decline with divergence from the ancestral marine stickleback phenotype. Competitive interactions affect partitioning of resources among different ecotypes and might lead to repeatability in resource use and phenotype distributions across different ecotype assemblages. Two Salmonid genera – Salvelinus and Coregonus – frequently diversify into assemblages of two to seven sympatric ecotypes in post-glacial lakes. We evaluated evidence for repeatability of niche occupation, phenotype distributions, and niche by phenotype relationships across assemblages in these genera. We found evidence for repeatable niche occupation and niche by phenotype relationships in Coregonus, but only repeatable niche by phenotype relationships in Salvelinus. While these studies do provide evidence for a role of competitive interactions in shaping natural selection and evolution, they also suggest that predictions from theory for evolutionary consequences of competition may not always be met in fish populations in post-glacial lakes.

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Hybridization is the process that mediates gene flow between sexually reproducing lineages. As such, the factors that determine the fitness of hybrids are critically important for speciation. Although hybridization between natural populations occurs in an explicitly ecological context, where hybrids must compete for resources and attract mates under prevailing ecological conditions, little attention has been paid to the mechanisms that mediate the ecological performance of hybrids. In Chapter 2, I expand upon existing models of speciation and find that standing variation improves hybrid fitness when parents adapt to similar environments, but reduces hybrid fitness when parents adapt to different environments. Chapter 3 systematically reviews the literature to report that F1 hybrids are often quite mismatched for divergent parental traits, and also uses a field experiment with sunflowers to show that this mismatch reduces fitness via seed count. Chapter 4 also uses data from the literature to demonstrate that divergent adaptation proceeds via pleiotropic alleles. In Chapter 5, I measure morphological traits in the lab to illustrate that the magnitude of trait `mismatch' in hybrids increases with the phenotypic distance between cross parents. Chapter 6 uses a pond experiment hybridizing 'parallel' ecotypes and reports that hybridization after parallel evolution results both in heterosis and hybrid breakdown. Finally, Chapter 7 uses DNA sequence data to illustrate that the genetic signature of hybrid incompatibilities - excess heterozygosity - is greater when stickleback hybrids are raised in ponds than when they are raised in aquaria. In sum, my thesis demonstrates that ecological selection against hybrids can result from rapid adaptation from standing variation, from mismatched trait combinations that evolve somewhat predictably, and can have a detectable genetic signature. Hybridization after parallel evolution, at least in stickleback, leads to relatively equal measures of hybrid breakdown and heterosis. Ecologically-mediated natural and sexual selection can clearly play a large role in mediating the fitness of hybrids - future work should aim to establish the importance of these processes for speciation more broadly.

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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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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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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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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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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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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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No abstract available.