Dolph Schluter

University of British Columbia | UBC · Biodiversity Research Centre and Zoology Department

Aim High repeatability among assemblages of closely related but ecologically distinct ecotypes implies predictability in evolution and assembly of communities. The conditions under which ecotype assemblages form predictably, and the reasons, have been little investigated. Here, we test whether repeatability declines as the number of ecotypes builds...

The vertebrate gut microbiota is a critical determinant of organismal function, yet it remains unclear if and how gut microbial communities affect host fitness under natural conditions. Here, we investigate associations between growth rate (a fitness proxy) and gut microbiota diversity and composition in a field experiment with threespine stickleba...

Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four...

Species competing for resources also commonly share predators. While competition often drives divergence between species, the effects of shared predation are less understood. Theoretically, competing prey species could either diverge or evolve in the same direction under shared predation depending on the strength and symmetry of their interactions....

Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built...

Speciation is the process by which barriers to gene flow evolve between populations. Although we now know that speciation is largely driven by natural selection, knowledge of the agents of selection and the genetic and genomic mechanisms that facilitate divergence is required for a satisfactory theory of speciation. In this essay, we highlight thre...

In contrast to ecological speciation, where reproductive isolation evolves as a consequence of divergent natural selection, speciation by parallel natural selection has been less thoroughly studied. To test whether parallel evolution drives speciation, we leveraged the repeated evolution of benthic and limnetic ecotypes of threespine stickleback fi...

A solitary population of consumers frequently evolves to the middle of a resource gradient and an intermediate mean phenotype compared to a sympatric pair of competing species that diverge to either side via character displacement. The forces governing the distribution of phenotypes in these allopatric populations, however, are little investigated....

It is thought that two species can coexist if they use different resources present in the environment, yet this assumes that species are completely reproductively isolated. We simulate coexistence outcomes for two sympatric species that are ecologically differentiated but have incomplete reproductive isolation. The consequences of interbreeding cru...

Where is evolution fastest? The biotic interactions hypothesis proposes that greater species richness creates more ecological opportunity, driving faster evolution at low latitudes, whereas the ‘empty niches’ hypothesis proposes that ecological opportunity is greater where diversity is low, spurring faster evolution at high latitudes. We tested the...

In contrast to ecological speciation, where reproductive isolation evolves as a consequence of divergent natural selection, speciation by parallel natural selection has been less thoroughly studied. To test whether parallel evolution drives speciation, we leveraged the repeated evolution of benthic and limnetic ecotypes of threespine stickleback fi...

Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are “intrinsic,” meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilit...

Why are speciation rates so variable across the tree of life? One hypothesis is that this variation is explained by how rapidly reproductive barriers evolve. We tested this hypothesis by conducting a comparative study of the evolution of bird song, a premating barrier to reproduction. Speciation in birds is typically initiated when geographically i...

Selection against mismatched traits in hybrids is the phenotypic analogue of intrinsic hybrid incompatibilities. Mismatch occurs when hybrids resemble one parent population for some phenotypic traits and the other parent population for other traits, and is caused by dominance in opposing directions or from segregation of alleles in recombinant hybr...

Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built...

Hybrid incompatibilities occur when interactions between opposite-ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are 'intrinsic', meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilit...

Global change is altering ecosystems at an unprecedented rate. The resulting shifts in species ranges and reproductive timing are opening the potential for hybridization between closely related species which could dramatically alter the genetic diversity, adaptive capacity and evolutionary trajectory of interbreeding taxa. Here, we used behavioural...

It is thought that two species can coexist if they use different resources present in the environment, yet this assumes that species are completely reproductively isolated. Closely related species often interbreed, raising the question of how this might affect coexistence. We model coexistence outcomes for two sympatric species that are ecologicall...

Significance The role of mutations of large effect in adaptive evolution is a question of enduring interest. Large-effect mutations were once seen as unlikely contributors to adaptation, but we now have numerous examples. A major shortcoming of the evidence is the lack of information on fitness effects of mutations. We conducted a quantitative trai...

Speciation is frequently initiated but rarely completed, a phenomenon hypothesized to arise due to the failure of nascent lineages to persist. Although a failure to persist often has ecological causes, key gaps exist between ecological and evolutionary theories that, if filled, would clarify when and why speciation succeeds or fails. Here, we apply...

The fitness of hybrids is a critical determinant of gene flow between hybridizing populations. If hybrid phenotypes change predictably as parental populations become increasingly divergent, this could provide insight into general mechanisms linking ecological divergence with reproductive isolation. In this study, we used threespine stickleback fish...

Compared to those of their parents, are the traits of first-generation (F1) hybrids typically intermediate, biased toward one parent, or mismatched for alternative parental phenotypes? To address this empirical gap, we compiled data from 233 crosses in which traits were measured in a common environment for two parent taxa and their F1 hybrids. We f...

Are biotic interactions stronger in the tropics? Here, we investigate nest predation in birds, a canonical example of a strong tropical biotic interaction. Counter to expectations, daily rates of nest predation vary minimally with latitude. However, life-history traits that influence nest predation have diverged between latitudes. For example, trop...

Where is evolution fastest? The biotic interactions hypothesis proposes that greater species richness creates more ecological opportunity, driving faster evolution at low latitudes, whereas the "empty niches" hypothesis proposes that ecological opportunity is greater where diversity is low, spurring faster evolution at high latitudes. Here we test...

Species interactions are widely thought to be strongest in the tropics, potentially contributing to the greater number of species at lower latitudes. Yet, empirical tests of this “biotic interactions” hypothesis remain limited and often provide mixed results. Here, we analyze 55 years of catch per unit effort data from pelagic longline fisheries to...

Understanding why some species accumulate more deleterious substitutions than others is an important question relevant in evolutionary biology and conservation sciences. Previous studies conducted in terrestrial taxa suggest that life history traits correlate with the efficiency of purifying selection and accumulation of deleterious mutations. Usin...

Background: Understanding why species go extinct has become a major goal of evolutionary biology. Recent studies have suggested that both species traits and rates of evolution might predict extinction probability in a changing world. Here, we tested whether species conservation status correlates with recent rates of niche evolution within their lin...

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalitie...

The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from the repeated divergence of lineages in association with repeated changes in the community of interacting species. Y...

Are first-generation (F 1 ) hybrids typically intermediate for all traits that differentiate their parents? Or are they similar to one parent for most traits, or even mismatched for divergent traits? Although the phenotype of otherwise viable and fertile hybrids determines their fate, little is known about the general patterns, predictors, and cons...

The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet,...

The genes underlying adaptations are becoming known, yet the causes of selection on genes—a key step in the study of the genetics of adaptation—remains uncertain. We address this issue experimentally in a threespine stickleback species pair showing exaggerated divergence in bony defensive armor in association with competition‐driven character displ...

Does competition influence patterns of coexistence between closely related taxa? Here we address this question by analyzing patterns of range overlap between related species of birds (‘sister pairs’) co‐occurring on a tropical elevational gradient. We explicitly contrast the behavioral dimension of interspecific competition (interference competitio...

As humans cause the redistribution of species ranges, hybridization between previously allopatric species is on the rise. Such hybridization can have complex effects on overall fitness of native species as new allelic combinations are tested. Widespread species introductions provide a unique opportunity to study selection on introgressed alleles in...

The biotic interactions hypothesis proposes that stronger interspecific interactions in the tropics drive faster evolution and speciation, giving rise to the latitudinal diversity gradient. This hypothesis has inspired many tests of whether certain biotic interactions are indeed stronger in the tropics. However, the possibility that populations hav...

Biotic interactions are potent, widespread causes of natural selection and divergent phenotypic evolution and can lead to genetic differentiation with gene flow among wild populations ("isolation by ecology") [1-4]. Biotic selection has been predicted to act on more genes than abiotic selection thereby driving greater adaptation [5]. However, diffi...

Adaptation often proceeds from standing variation, and natural selection acting on pairs of populations is a quantitative continuum ranging from parallel to divergent. Yet, it is unclear how the extent of parallel genetic evolution during adaptation from standing variation is affected by the difference in the direction of selection between populati...

Does competition influence patterns of coexistence between closely related taxa? Here we address this basic question in ecology by analyzing patterns of range overlap between related bird species (sister pairs) distributed along a Neotropical elevational gradient. We explicitly contrast the behavioral dimension of interspecific competition (interfe...

DNA breakage and adaptation Adaptation to new environments often occurs in similar ways across different colonization events. Stickleback fish represent a classic example of this, in which repeated colonizations of freshwater have resulted in the loss of pelvic hind fins. Previous work has shown that a pelvic enhancer gene is involved. Xie et al. n...

Many outstanding questions about speciation are difficult to test empirically because of a lack of suitable study systems. Here, we highlight studies of evolutionary ecology in urban environments to argue that cities provide ideal conditions that can be leveraged to study the speciation process. Considering general findings from these studies, we d...

Adaptation often proceeds via the sorting of standing variation, and natural selection acting on pairs of populations is a quantitative continuum ranging from parallel to divergent. Yet, it is unclear how the extent of parallel genetic evolution during adaptation from standing variation is affected by the difference in the direction of selection be...

Ionoregulation in the euryhaline killifish Fundulus heteroclitus has been intensively studied over the last two decades using a variety of techniques. However, there has been limited use of pharmacological inhibitors to identify proteins involved in ion transport for this species. In this study, we used a range of pharmacological inhibitors (EIPA,...

Understanding the mechanisms by which the abiotic and biotic requirements of species, or ecological niches, change over time is a central issue in evolutionary biology. Niche evolution is poorly understood at both the macroecological and macroevolutionary scales, as niches can shift over short periods of time but appear to change more slowly over l...

In the version of this Article originally published, in Fig. 3a the first boundary was incorrectly labelled the “K/T boundary”; it should have read the “K/Pg boundary”. The two equations in the main text were incorrectly omitted from the HTML. In the description of the posterior distribution of an ancestral state, the normal distribution was incorr...

Character displacement is one of the most studied phenomena in evolutionary biology, yet research has narrowly focused on demonstrating whether or not displacement has occurred. We propose a new experimental approach, adopted from the coexistence literature, that directly measures interspecific competition among sympatric and allopatric populations...

Ecological speciation with gene flow is widespread in nature [1], but it presents a conundrum: how are associations between traits under divergent natural selection and traits that contribute to assortative mating maintained? Theoretical models suggest that genetic mechanisms inhibiting free recombination between loci underlying these two types of...

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This "song learning" hypothesis predicts that 1) differences in song traits evolve faster in song learners, and 2) behavioral discrimin...

Adaptation to new environments often occurs in the face of gene flow. Under these conditions,gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potent...

Global patterns of biodiversity are influenced by spatial and environmental variations in the rate at which new species form. We relate variations in speciation rates to six key patterns of biodiversity worldwide, including the species-area relationship, latitudinal gradients in species and genetic diversity, and between-habitat differences in spec...

Mechanisms of natural selection can be identified using experimental approaches. However, such experiments often yield non-significant effects and imprecise estimates of selection due to low power and small sample sizes. Combining results from multiple experimental studies might produce an aggregate estimate of selection that is more revealing than...

Evolution is recognized as the source of all organisms, and hence many ecosystem services. However, the role that contemporary evolution might play in maintaining and enhancing specific ecosystem services has largely been overlooked. Recent advances at the interface of ecology and evolution have demonstrated how contemporary evolution can shape eco...

Background: Studying how trophic traits and niche use are related in natural populations is important in order to understand adaptation and specialization. Here, we describe trophic trait diversity in twenty-five Norwegian freshwater threespine stickleback populations and their putative marine ancestor, and relate trait differences to postglacial...

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matchi...

Strong ecological selection on a genetic locus can maintain allele frequency differences between populations in different environments, even in the face of hybridization. When alleles at divergent loci come into tight linkage disequilibrium, selection acts on them as a unit and can significantly reduce gene flow. For populations interbreeding acros...

The extent to which convergent adaptation to similar ecological niches occurs by a predictable genetic basis remains a fundamental question in biology. Threespine stickleback fish have undergone an adaptive radiation in which ancestral oceanic populations repeatedly colonized and adapted to freshwater habitats. In multiple lakes in British Columbia...

The addition of predators can play a key role in structuring ecological communities through both consumptive and non-consumptive effects. Stocking of piscivorous fish in lakes and similar experimental introductions have provided fundamental evidence in support of trophic cascade theory. Yet, the impact of piscivore addition on cross ecosystem subsi...

Young species are highly prone to extinction via increased gene flow after human-caused environmental changes [1-6]. This mechanism of biodiversity loss, often termed reverse speciation or introgressive extinction, is of exceptional interest because the parent species are typically highly differentiated ecologically. Reverse speciation events are p...

Evolutionary hypotheses to explain the greater numbers of species in the tropics than the temperate zone include greater age and area, higher temperature and metabolic rates, and greater ecological opportunity. These ideas make contrasting predictions about the relationship between speciation processes and latitude, which I elaborate and evaluate....

Intraguild predation is a common ecological interaction that occurs when a species preys upon another species with which it competes. The interaction is potentially a mechanism of divergence between intraguild prey populations, but it is unknown if cases of character shifts in intraguild prey are an environmental or evolutionary response. We invest...

How predictable is the genetic basis of phenotypic adaptation? Answering this question begins by estimating the repeatability of adaptation at the genetic level. Here, we provide a comprehensive estimate of the repeatability of the genetic basis of adaptive phenotypic evolution in a natural system. We used quantitative trait loci (QTL) mapping to d...

Strong ecological selection on a genetic locus can maintain allele frequency differences between populations in different environments, even in the face of hybridization. When alleles at divergent loci come into tight linkage disequilibria, selection acts on them as a unit and can significantly reduce gene flow. For populations interbreeding across...

Abstract When a signature of natural selection is discovered on a gene that is pleiotropic or in tight linkage with other genes, it is challenging to determine which of the affected phenotypes is under selection. One way to make progress is to employ methods for analyzing natural selection on correlated traits, including both genotype and phenotype...

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Significance How body pattern evolves in nature remains largely unknown. Although recent progress has been made on the molecular basis of losing morphological features during adaptation to new environments (regressive evolution), there are few well worked out examples of how morphological features may be gained in natural species (constructive evol...

Uncovering factors that shape variation in brain morphology remains a major challenge in evolutionary biology. Recently, it has been shown that brain size is positively associated with level of parental care behavior in various taxa. One explanation for this pattern is that the cognitive demands of performing complex parental care may require incre...

Table S1. Site information and number of threespine sticklebacks collected at the five locations examined in this study.

Figure S1. Standard lengths of male and female fish from seven Canadian populations of threespine stickleback.

Figure S2. Dry brain weights for two Canadian populations of sticklebacks (population information available in Table S1).

Ecological differences often evolve early in speciation as divergent natural selection drives adaptation to distinct ecological niches, leading ultimately to reproductive isolation. Although this process is a major generator of biodiversity, its genetic basis is still poorly understood. Here we investigate the genetic architecture of niche differen...

The role of natural selection in the maintenance of genetic variation in wild populations remains a major problem in evolution. The influence of disruptive natural selection on genetic variation is especially interesting because it might lead to the evolution of assortative mating or dominance [1, 2]. In theory, variation can persist at a gene unde...

Understanding the genetic architecture of evolutionary change remains a long-standing goal in biology. In vertebrates, skeletal evolution has contributed greatly to adaptation in body form and function in response to changing ecological variables like diet and predation. Here we use genome-wide linkage mapping in threespine stickleback fish to inve...

The evolution of ecological divergence in closely related species is a key component of adaptive radiation. However, in most examples of adaptive radiation the mechanistic basis of ecological divergence remains unclear. A classic example is seen in the young benthic and limnetic stickleback species pairs of British Columbia. In each pair the benthi...

The role of natural selection in promoting reproductive isolation has received substantial renewed interest within the last two decades. As a consequence, the study of ecological speciation has become an extremely productive research area in modern evolutionary biology. Recent innovations in sequencing technologies offer an unprecedented opportunit...

Reproductive isolation is central to the study of speciation. Multiple isolating barriers may prevent species from hybridizing, although their individual strength and the interactions between them are rarely measured. We quantified habitat isolation in a recently diverged threespine stickleback species pair (Gasterosteus aculeatus complex) and cont...

Mate choice by phenotype matching, whereby individuals prefer a mate whose phenotype is similar to their own, should facilitate speciation with gene flow. This is because the genes that control mate signal (the phenotype being matched) also determine the preferred mate signal ("mate preference"). Speciation is made even easier if phenotype matching...

Species' ecology and evolution can have strong effects on communities. Both may change concurrently when species colonize a new ecosystem. We know little, however, about the combined effects of ecological and evolutionary change on community structure. We simultaneously examined the effects of top-predator ecology and evolution on freshwater commun...

Genomic and genetic methods allow investigation of how frequently the same genes are used by different populations during adaptive evolution, yielding insights into the predictability of evolution at the genetic level. We estimated the probability of gene reuse in parallel and convergent phenotypic evolution in nature using data from published stud...

Transition of an evolving population to a new adaptive optimum is predicted to leave a signature in the distribution of effect sizes of fixed mutations. If they affect many traits (are pleiotropic), large effect mutations should contribute more when a population evolves to a farther adaptive peak than to a nearer peak. We tested this prediction in...

Phenotypic plasticity may be favored in generalist populations if it increases niche width, even in temporally constant environments. Phenotypic plasticity can increase the frequency of extreme phenotypes in a population and thus allow it to make use of a wide resource spectrum. Here we test the prediction that generalist populations should be more...

Intraguild predation--competition and predation by the same antagonist--is widespread, but its evolutionary consequences are unknown. Intraguild prey may evolve antipredator defenses, superior competitive ability on shared resources, or the ability to use an alternative resource, any of which may alter the structure of the food web. We tested for e...

Mate choice by phenotype matching, whereby individuals prefer a mate whose phenotype is similar to their own, should facilitate speciation with gene flow. This is because the genes that control mate signal (the phenotype being matched) also determine the preferred mate signal (‘mate preference’). Speciation is made even easier if phenotype matching...

Genes underlying repeated adaptive evolution in natural populations are still largely unknown. Stickleback fish (Gasterosteus aculeatus) have undergone a recent dramatic evolutionary radiation, generating numerous examples of marine-freshwater species pairs and a small number of benthic-limnetic species pairs found within single lakes [1]. We have...

Examining differences in colour plasticity between closely-related species in relation to the heterogeneity of background colours found in their respective habitats may offer important insight into how cryptic colour change evolves in natural populations. In the present study, we examined whether nonbreeding dorsal body coloration has diverged betw...

Measuring the strength of natural selection is tremendously important in evolutionary biology, but remains a challenging task. In this work, we analyse the characteristics of selection for a morphological change (lateral-plate reduction) in the threespine stickleback Gasterosteus aculeatus. Adaptation to freshwater, leading with the reduction or lo...

Gillman et al. [[1][1]] test the notion that rates of molecular evolution are accelerated in small-bodied mammal species inhabiting geographical areas with warmer ambient temperatures. Their methodology involved estimation of many phylogenetic trees each consisting of a mammal sister species pair

The long-standing goal of finding genes causing reproductive isolation is being achieved. To better link the genetics with the process of speciation, we propose that 'speciation gene' be defined as any gene contributing to the evolution of reproductive isolation. Characterizing a speciation gene involves establishing that the gene affects a compone...

Growing knowledge of the molecular basis of adaptation in wild populations is expanding the study of natural selection. We summarize ongoing efforts to infer three aspects of natural selection--mechanism, form and history--from the genetics of adaptive evolution in threespine stickleback that colonized freshwater after the last ice age. We tested a...

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populatio...