Biology subjects

Schluter, D.

Publications and source records attributed to Schluter, D..

16 recordsLinked to original sources

bioRxiv2025

Rapid and repeated evolution of myosin copy number in threespine stickleback

Copy number variants at genomic loci evolve at a high rate, are linked to many different diseases, and play a role in adaptive evolution in humans and other organisms. Here we show that stickleback fish from freshwater environments have rapidly and repeatedly evolved an expanded number of copies of a gene family involved in muscle development, Myosin Heavy Chain 3 Cluster C (MYH3C), compared to marine populations. Differences in copy number between marine and freshwater fish are maintained even in the presence of gene flow, suggesting that MYH3C changes represent adaptive divergence between ecotypes. Copy number expansion occurs by tandem duplication of MYH3C coding and regulatory regions on the stickleback sex chromosome. We identify a muscle regulatory enhancer within the expanded MYH3C region and show that elevated copy number is associated with developmental and tissue-specific increases in corresponding mRNA expression levels in skeletal muscle. Common MYH3C clusters include 3-, 4-, 5-, and 6-copy variants that likely evolved through a combination of microhomology-mediated break repair and non-allelic homologous recombination. Our results provide a new example of copy number changes in a wild species and identify CNVs as potential "hotspots" of repeated adaptive evolution.

evolutionary biology↗

bioRxiv2025

Species interactions, divergence, and the rapid evolution of ecological sexual dimorphism in threespine sticklebacks

Variation in ecological sexual dimorphism (ESD), defined as differences between the sexes in ecologically-relevant traits, is a common feature of adaptive radiation, yet its causes remain unclear. Competition between the sexes for alternative resources can promote evolution of ESD when interspecific competition is reduced (competition hypothesis). Alternatively, sex-specific selection on ecological traits might weaken under strong directional selection in new environments (divergence hypothesis). We tested these hypotheses via their expected evolutionary outcomes in threespine stickleback populations from southwestern Canada. We found striking among-population variation in magnitude of ESD. Consistent with the divergence hypothesis, dimorphism along the main axis of body shape variation was reduced in recently derived freshwater populations compared to their contemporary marine ancestor. However, dimorphism only weakly declined with increasing phenotypic divergence. Average dimorphism along major freshwater body shape axes was similar between solitary populations and those coexisting with a competing species, contrary to the competition hypothesis. Instead, sympatry with a Benthic ecotype led to increased sexual size dimorphism in Limnetics, and total shape dimorphism was elevated in the sympatric stickleback species compared with solitary populations. In contrast to the mechanisms considered in existing theory, interactions in sympatry might produce elevated ESD by generating novel sex-specific selection pressures.

evolutionary biology↗

bioRxiv2025

Genetic divergence in the absence of strong ecological differences between coexisting white and common Atlantic marine sticklebacks

Identifying taxa in the earliest phases of speciation is critical for understanding how reproductive isolation arises. In Nova Scotia, Canada, "white" threespine sticklebacks co-occur with common marine sticklebacks but differ in nuptial coloration, nesting behavior, and parental care, raising the possibility that they represent a nascent species. We combined population genomics, morphometrics, and stable isotope analysis to test whether white sticklebacks represent a distinct lineage and whether they have diverged along ecological axes as in other stickleback populations. Genotyping-by-sequencing revealed that male and female white sticklebacks form a genetic cluster distinct from sympatric common sticklebacks with evidence of ongoing gene flow yet with very low overall genomic divergence (FST {approx} 0.01). Genetic differences were distributed across many loci rather than localized to a single genomic region. Morphological and isotopic analyses revealed no differences in most classic ecological traits (body shape, armor, gill rakers, or trophic niche). Instead, whites are smaller-bodied, paler, and exhibit shorter spines, reduced testes size, and smaller but more numerous eggs compared to common sticklebacks. These results indicate that white sticklebacks are genetically distinct from the common Atlantic threespine stickleback but have not diverged conspicuously in their ecology, suggesting that their differentiation is driven by reproductive and sexual traits rather than trophic specialization. The white stickleback thus represents a promising new system for investigating the interplay of sexual selection, reproductive strategy, and gene flow in the early stages of speciation.

evolutionary biology↗

bioRxiv2025

Dynamics of infection and immunity over 50 years as marine stickleback adapt to freshwater

When a species colonizes a new environment, it may encounter new parasites to which its immune system is poorly adapted. After an initial spike in infection rates in the naive founder population, the host may subsequently evolve increased immunity thereby reducing infection rates. Here, we present an example of this eco-evolutionary process, in a population of threespine stickleback (Gasterosteus aculeatus) that was founded in Heisholt Quarry, a man-made quarry pond, in 1967. Marine stickleback rarely encounter Schistocephalus solidus tapeworms (which require freshwater to hatch), and so remain highly susceptible to infection. Initially, introduced marine fish were heavily infected by S.solidus. They exhibited low levels of fibrosis, a heritable immune trait which some genotypes activate in response to infection, thereby suppressing tapeworm growth and viability. By the 1990s, the Heisholt Quarry population exhibited high rates of fibrosis, which partly suppressed S.solidus infection. This increased immune response led to reduced infection rates and the tapeworm was apparently extirpated by 2021. Because fibrosis has a strong genetic basis in other stickleback populations, we infer that the newly founded stickleback-parasite interaction exhibit an eco-evolutionary process of increased immunity that e_ectively reduced infection. The infection and immune dynamics documented here closely match those expected from a simple eco-evo dynamic model presented here. IMPACT SUMMARYParasite-host relationships are a great framework within which to study the mechanisms driving evolutionary change, both in terms of ecological dynamics, selection pressures, and the phenotypic basis of adaptation to environmental change. One classic example of adaptation is the loss of armor plating as marine stickleback fish colonize freshwater habitats. However, the parasitological and immunological adaptations in new freshwater populations are less clear. When marine fish colonize freshwater they encounter an unfamiliar tapeworm parasite, Schistocephalus solidus, to which they are poorly adapted. Many (but not all) freshwater populations evolve an inducible fibrosis response to S.solidus, a build-up of scar tissue that limits parasite growth and survival. However, we did not know the time frame over which marine fish, invading freshwater, will evolve this immune trait. To resolve this, we tracked the eco-evolutionary dynamics of Schistocephalus solidus tapeworm infection and the fibrosis immune response over 50 years, in an artificial quarry pond populated by susceptible marine fish in 1967. We show that infection rates were initially high, as the marine fish encountered a freshwater parasite to which they were not adapted. Fibrosis rates subsequently increased, reducing the infection rates and by 2021 S.solidus was apparently eliminated. This process matches a simple eco-evolutionary model of an inducible immune response, and provides a clear example of how hosts can adapt to and suppress novel parasites. Although fibrosis is typically viewed as an immune pathology contributing to disease in humans, we show that in stickleback it has a key adaptive value in protection against helminth infection.

evolutionary biology↗

bioRxiv2023

A positive association between gut microbiota diversity and vertebrate host performance in a field experiment

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 stickleback fish (Gasterosteus aculeatus). We detected on average 63% more bacterial taxa in the guts of high-fitness fish compared to low-fitness fish (i.e., higher -diversity), suggesting that higher diversity promotes host growth. The microbial communities of high-fitness fish had higher similarity (i.e., lower {beta}-diversity) than low-fitness fish, supporting the Anna Karenina principle-- that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our findings provide a basis for functional tests of the fitness consequences of host-microbiota interactions. Significance statementThe vertebrate gut microbiota is important for many aspects of their hosts biology--such as nutrient metabolism and defense against pathogens--that could ultimately affect host fitness. However, studies investigating the effects of gut microbiota composition on vertebrate host fitness under natural conditions remain exceedingly rare. We tested for associations between gut microbiota diversity and growth rate (a fitness proxy) in threespine stickleback fish reared in large outdoor ponds. We found evidence that a more diverse gut microbiota was predictive of higher growth rate and therefore increased host fitness. Notably, high-fitness fish had higher gut microbiota similarity to one another than did low-fitness fish, providing experimental evidence for the Anna Karenina principle--that there are fewer ways to have a functional microbiota than a dysfunctional microbiota--as it relates to host fitness.

evolutionary biology↗

bioRxiv2022

Heterosis counteracts hybrid breakdown to forestall speciation by parallel natural selection

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 fish and estimated fitness for pure crosses and within-ecotype hybrids in semi-natural ponds and in laboratory aquaria. In ponds, we detected hybrid breakdown in both ecotypes but this was counterbalanced by heterosis and the strength of post-zygotic isolation was nil. In aquaria, we detected heterosis only in limnetic crosses and breakdown in neither ecotype, suggesting that hybrid incompatibilities are environment-dependent for both ecotypes and that heterosis is environment-dependent in benthic crosses. Heterosis and breakdown were 3x greater in limnetic crosses than in benthic crosses, contrasting the prediction that the fitness consequences of hybridization should be greater in crosses among more derived ecotypes. Consistent with a primary role for stochastic processes, patterns differed among crosses between populations from different lakes. Yet, we observed qualitatively similar patterns of heterosis and hybrid breakdown in benthic crosses and limnetic crosses when averaging the lake pairs, suggesting that the outcome of hybridization is repeatable in a general sense.

evolutionary biology↗

bioRxiv2021

Chromosome-scale genome assembly of the brown anole (Anolis sagrei), a model species for evolution and ecology

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 on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a new, highly complete chromosome-scale genome assembly for the brown anole, Anolis sagrei - a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue.

genomics↗

bioRxiv2021

Genetic evidence for environment-dependent hybrid incompatibilities in threespine stickleback

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 incompatibilities, but tests of this hypothesis are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (semi-natural experimental ponds) or the laboratory (aquaria). We tested for differences in excess heterozygosity between these two environments at ancestry informative loci--a genetic signature of selection against incompatibilities. We found that excess ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Previous results from F1 hybrids in the field suggest that pond-specific (single-locus) heterosis is unlikely to explain this finding. Our study suggests that, in stickleback, a coarse signal of environment-dependent hybrid incompatibilities is reliably detectable and that extrinsic incompatibilities have evolved before intrinsic incompatibilities.

evolutionary biology↗

bioRxiv2021

Hybridization and the coexistence of species

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 model coexistence outcomes for two sympatric species that are ecologically differentiated but have incomplete reproductive isolation. The consequences of interbreeding depend crucially on hybrid fitness. When hybrid fitness is high, just a small rate of hybridization can lead to collapse of two species into one. Low hybrid fitness can cause population declines, making extinction of one or both species likely. High intrinsic growth rates result in higher reproductive rates when populations are below carrying capacity, reducing the probability of extinction and increasing the probability of stable coexistence at moderate levels of assortative mating and hybrid fitness. Very strong but incomplete assortative mating can induce low hybrid fitness via a mating disadvantage to rare genotypes, and this can stabilize coexistence of two species at high but incomplete levels of assortative mating. Given these results and evidence that it may take many millions of years of divergence before related species become sympatric, we postulate that coexistence of closely-related species is more often limited by insufficient assortative mating than by insufficient ecological differentiation.

ecology↗

bioRxiv2020

Adaptive divergence and the evolution of hybrid phenotypes in threespine stickleback

Hybrid fitness can be negatively impacted by trait mismatch, whereby hybrids resemble one parent population for some phenotypic traits and the other parent population for other traits. In this study, we used threespine stickleback fish (Gasterosteus aculeatus L.) to test whether trait mismatch in hybrids increases with the magnitude of phenotypic divergence between parent populations. We measured morphological traits in parents and hybrids in crosses between a marine population representing the ancestral form and twelve freshwater populations that have diverged from this ancestral state to varying degrees according to their environments. We found that trait mismatch was greater in more divergent crosses for both F1 and F2 hybrids. In the F1, the divergence-mismatch relationship was caused by traits having dominance in different directions whereas it was caused by segregating phenotypic variation in the F2. Selection against mismatched traits is an ecological analogue to selection against intrinsic hybrid incompatibilities, and our results imply that extrinsic hybrid incompatibilities accumulate predictably as phenotypic divergence proceeds.

evolutionary biology↗

bioRxiv2020

The latitudinal gradient in the rate of evolution of a biotic interaction trait

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 tested these contrasting predictions by analyzing rates of bird beak evolution for a global dataset of 1141 sister pairs of birds. Beak size evolves at similar rates across latitudes, while beak shape evolves faster in the temperate zone, consistent with the empty niches hypothesis. We show in a meta-analysis that trait evolution and recent speciation rates are faster in the temperate zone, while rates of molecular evolution are slightly faster in the tropics. Our results suggest that drivers of evolutionary diversification are more potent at higher latitudes, thus calling into question multiple hypotheses invoking faster tropical evolution to explain the latitudinal diversity gradient.

evolutionary biology↗

bioRxiv2019

Patterns, predictors, and consequences of dominance in hybrids

Are first-generation (F1) 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 consequences of phenotype expression in hybrids. To address this empirical gap, we compiled data from nearly 200 studies where traits were measured in a common environment for two parent populations and F1 hybrids. We find that individual traits are typically halfway between the parental midpoint and one parental value (i.e., hybrid trait values are typically 0.25 or 0.75 if parents values are 0 & 1). When considering pairs of traits together, a hybrids multivariate phenotype tends to resemble one parent (pairwise parent-bias) about 50 % more than the other while also exhibiting a similar magnitude of trait mismatch due to different traits having dominance in conflicting directions. We detect no phylogenetic signal nor an effect of parental genetic distance on dominance or mismatch. Using data from an experimental field planting of recombinant hybrid sunflowers--where there is among-individual variation in dominance and mismatch due to segregation of divergent alleles--we illustrate that pairwise parent-bias improves fitness while mismatch reduces fitness. Importantly, the effect of mismatch on fitness was stronger than that of pairwise parent-bias. In sum, our study has three major conclusions. First, hybrids between ecologically divergent natural populations are typically not phenotypically intermediate but rather exhibit substantial mismatch while also resembling one parent more than the other. Second, dominance and mismatch are likely determined by population-specific processes rather than general rules. Finally, selection against hybrids likely results from both selection against somewhat intermediate phenotypes and against mismatched trait combinations.

evolutionary biology↗

bioRxiv2019

Parallel changes in gut microbiome composition and function in parallel local adaptation and speciation

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, relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we utilize three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification.

evolutionary biology↗

bioRxiv2019

Adaptation and latitudinal gradients in species interactions: nest predation in birds

The "biotic interactions" hypothesis--that stronger interspecific interactions in the tropics drive faster evolution and speciation, giving rise to the latitudinal diversity gradient--has inspired many tests of whether certain biotic interactions are indeed stronger in the tropics. However, the possibility that populations have adapted to latitudinal differences in species interactions, blunting effects on evolutionary rates, has been largely ignored. Here we show that mean rates of nest predation experienced by land birds vary minimally with latitude in the Western Hemisphere. This result is surprising because nest predation in birds is a canonical example of a strong tropical biotic interaction. We explain our finding by demonstrating that (1) rates of nest predation are in fact higher in the tropics, but only when controlling for the length of the nesting period, (2) long nesting periods are associated with reduced predation rates, and (3) tropical birds have evolved particularly long nesting periods. We suggest this is a case example of how adaptation to a biotic interaction can alter observed latitudinal gradients in interaction strength, potentially equalizing evolutionary rates among latitudes. More broadly, we advocate for tests of the biotic interactions hypothesis to consider both latitudinal patterns in interaction strength and evolutionary responses to these interactions.

evolutionary biology↗

bioRxiv2019

Behavior influences range limits and patterns of coexistence across an elevational gradient in tropical bird diversity

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 (interference competition) with similarity in resource acquisition traits (exploitative competition). We find that behavioral interactions are generally important in setting elevational range limits and preventing coexistence of closely related species. Specifically, close relatives that defend year-round territories tend to live in non-overlapping elevational distributions, while close relatives that do not defend territories tend to broadly overlap in distribution. In contrast, neither similarity in beak morphology nor evolutionary relatedness was associated with patterns of range limitation. Our main result is that interference competition can be an important driver of species ranges at the scale of entire diverse assemblages. Consequently, we suggest that behavioral dimensions of the niche should be more broadly incorporated in macroecological studies.

ecology↗

bioRxiv2018

Patterns of speciation and parallel genetic evolution under adaptation from standing variation

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 between populations. Nor is it clear whether the availability of standing variation for adaptation affects progress toward speciation in a manner that depends on the difference in the direction of selection. We conducted a theoretical study investigating these questions and have two primary findings. First, the extent of parallel genetic evolution between two populations is expected to rapidly decline as the difference in their directions of selection increases from fully parallel toward divergent, and this decline occurs more rapidly in organisms with greater trait dimensionality. This rapid decline results because seemingly small differences in the direction of selection cause steep reductions in the fraction of alleles that are beneficial in both populations. For example, populations adapting to optima separated by an angle of 33{degrees} have only 50% of potentially beneficial alleles in common (for a case of five trait dimensions). Second, we find that adaptation from standing variation leads to higher ecologically-dependent hybrid fitness under parallel selection, relative to when adaptation is from new mutation only. This occurs because genetic parallelism based on standing variation reduces the phenotypic segregation variance in hybrids when parents adapt to similar environments. In contrast, under divergent selection, the pleiotropic effects of alternative alleles fixed from standing variation change the major axes of phenotypic variation in hybrids and reduce their fitness in parental habitats. We conclude that adaptation from standing genetic variation is expected to slow progress toward speciation via parallel natural selection and can facilitate progress toward speciation via divergent natural selection.\n\nImpact summaryIt is increasingly clear that much of adaptation, especially that which occurs rapidly, proceeds from the sorting of ancestral standing variation rather than complete reliance on de novo mutation. In addition, evolutionary biologists are increasingly embracing the fact that the difference in the direction of natural selection on pairs of populations is a quantitative continuum ranging from completely parallel to completely divergent. In this article, we ask two questions. First, how does the degree of genetic parallelism--here, adaptation using the same alleles in allopatric populations--depend on the differences in the direction of natural selection acting on two populations, from parallel (0{degrees}) to divergent (180{degrees})? And second, how does adaptation from standing variation affect progress toward speciation, and does its effect depend on the direction of natural selection? We develop theory to address these questions. We first find that very small differences in the direction of selection (angle) can largely preclude genetic parallelism. Second, we find that adaptation from standing variation has implications for speciation that change along the continuum from parallel to divergent selection. Under parallel selection, high genetic parallelism causes inter-population hybrids to have high mean fitness when their parents adapt from standing variation. As selection tends toward divergent, adaptation from standing variation is less beneficial for hybrid fitness and under completely divergent selection causes inter-population hybrids to have lower mean fitness than when adaptation was from new mutation alone. In sum, our results provide general insight into patterns of genetic parallelism and speciation along the continuum of parallel to divergent natural selection when adaptation is from standing variation.

evolutionary biology↗