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Biology subjects

Hendry, A. P.

Publications and source records attributed to Hendry, A. P..

13 recordsLinked to original sources

Disassortative mating in replicated secondary contact experiments in nature

Ecological speciation is now regarded as one of the primary processes by which new species are generated. Adaptive divergence in allopatry begins this process, but it is often unclear when and how mechanisms that promote reproductive isolation, such as assortative mating and selection against hybrids, evolve. Here, we test for evidence of these mechanisms across replicated secondary contact experiments in natural settings. We introduced four to eight allopatric populations of threespine stickleback (Gasterosteus aculeatus), in both single-ecotype and mixed-ecotype treatments, into nine natural lakes, after which we inferred mating patterns by genotyping the resulting F1 generation. Contrary to expectations from the literature, we found no evidence of assortative mating or partial reproductive isolation among the introduced source populations. Instead, we detected evidence of disassortative mating by source population in three lakes and some evidence of disassortative mating by ecotype in one lake. These mating patterns were both context-dependent and population-dependent, varying substantially across lakes receiving the same source populations, and with some source populations generally displaying greater tendencies for disassortment. The absence of positive assortative mating in any replicate demonstrates that adaptive divergence in allopatry alone might be insufficient to generateassortative mating in many cases, while the possibility of disassortative mating in these contexts poses an additional hurdle on the path toward speciation.

evolutionary biology↗

Intrinsic fitness differences outweigh environmental matching in shaping introduction outcomes in nature

Species introductions and transplants offer powerful contexts to understand evolutionary patterns and processes, and they are increasingly critical for conservation. However, introduction success varies widely, and predicting outcomes remains challenging. Introducing multiple source populations should increase the chance of success, while also providing an opportunity to explore the factors that predict success of individual source populations in the same environment. We used replicated, mixed-population introductions of >12,000 threespine stickleback (Gasterosteus aculeatus) to test whether source population success could be predicted by environmental matching between source and recipient environments and/or by intrinsic source population characteristics. We introduced four to eight source populations of stickleback into each of nine natural lakes and tracked their relative success over the following two years (up to two generations). Source population success was largely consistent across lakes, despite divergent environmental conditions. These results point to the importance of intrinsic source population characteristics rather than environmental matching in predicting introduction success in natural settings. Source populations that were consistently successful tended to have greater stress tolerance (mortality rate during translocation) and higher genetic diversity, though these relationships were not conclusive. Our study highlights the value of considering factors that generate fitness differences independent of environmental contexts in predicting ecological and evolutionary dynamics and planning conservation programs. Significance StatementPredicting which populations will succeed when introduced to new environments is a central challenge in ecology, evolution, and conservation. Environmental conditions are often assumed to be crucial in determining which populations succeed, given the expectation that populations preadapted to local conditions should perform best. We test this assumption by introducing >12,000 threespine stickleback fish from up to eight source populations into nine natural lakes spanning diverse environmental conditions. We show that the relative success of individual source populations was remarkably consistent across lakes and environmental conditions, indicating that some populations are intrinsically better suited to introductions. Our findings underscore the importance of considering intrinsic population characteristics alongside environmental conditions when predicting ecological and evolutionary outcomes and guiding conservation efforts.

evolutionary biology↗

Lake size shapes the relationship between body mass and gut microbiota in threespine stickleback (Gasterosteus aculeatus)

Host-microbe interactions are shaped by both host and environmental factors. However, little is known about how host-microbe interactions vary across populations within a species. Here, we characterized the gut microbiota of 191 wild threespine stickleback fish (Gasterosteus aculeatus) from six populations from Alaskan lakes spanning a gradient of surface area. We tested how environmental context (lake size and ecotype) and host traits (sex, body mass, gravidity, Schistocephalus solidus (S. solidus) infection, and fibrosis) influence stickleback gut microbial composition using 16S rRNA gene sequencing. We found that the lake surface area strongly predicted fish gut microbial alpha diversity. Fish from intermediate-sized lakes harbored significantly more diverse microbiota than those from small and large lakes, independent of ecotype. Body mass was associated with gut microbial diversity. Model-predicted marginal effects from the mass and lake surface area interaction analysis showed that the association between fish mass and microbial alpha diversity was strongly negative in the smallest lakes, weakest in intermediate-sized lakes, and strongly positive in the largest lakes. In addition, sex and S. solidus infection were significantly associated with gut microbiota alpha and beta diversity, whereas fibrosis and gravidity showed minimal effects. Differential abundance analysis revealed lake size-dependent associations between body mass and individual taxa. Together, these results demonstrate that both habitat context and host variation interactively shape stickleback gut microbial communities in the wild. Integrating lake-level and individual-level analyses reveals how ecological setting modulates host-microbe associations, offering insights into the role of the gut microbiota in host adaptation and population divergence.

microbiology↗

Fish Show Genetic Evolutionary Responses to River Regulation

Eco-hydraulics traditionally aims at managing riverine systems in a semi-natural state while meeting human demands, assuming aquatic species are static. However, evidence of rapid evolution suggests that ignoring evolutionary dynamics of fish species might limit long-term effectiveness of eco-hydraulics frameworks. It remains unclear how freshwater fish adapt to human perturbation. Why are some fish populations more resilient to human perturbation than others? What are the genetic mechanisms behind it? To answer these questions, we genotyped eleven populations of three-spined stickleback in a regulated river system and collected data on river morphology, connectivity, flow regimes, physico-chemistry and parasite abundance through a combination of field surveys and modelling. Gene-environment association analysis detected strong signals of genetic divergence associated with hydraulic features. Gene ontology analysis revealed evolutionary responses that primarily involve functions in the nervous and sensory systems. These findings demonstrate that fish can evolve in response to river regulation, highlighting the need to transition from eco-hydraulics toward eco-evo-hydraulics.

evolutionary biology↗

Behavior Outpaces Form when Linking Traits to Ecological Responses within Populations: A Meta-Analysis

Intraspecific variability is fundamental to ecology, yet we still know remarkably little about what governs the strength of the associations between traits expressed by individuals and ecological dynamics. To explore this overlooked aspect of diversity, we asked whether the strength of correlations between traits and a wide spectrum of ecological responses could differ (i) between intraspecific levels (among vs. within populations), (ii) among ecological responses across levels of biological organization (from ecological performance to ecosystem functioning), and (iii) among trait types (morphology, physiology, and behavior). We performed a meta-analysis synthesizing over a thousand effect sizes from nearly two hundred studies spanning approximately a hundred animal species across a broad range of traits and ecological responses. The average effect size was |r| = 0.26 (95% confidence interval: 0.21 - 0.30). At the individual level, effect sizes were larger for ecological performance (foraging, diet) than for fitness (reproduction), and tended to be larger for community responses (e.g., community composition of surrounding organisms). Physiology and behavior showed larger effect sizes than morphology. Our meta-analysis not only confirms that intraspecific trait variability is central to ecological dynamics, but also highlights physiology and behavior as key traits for unraveling the ecological consequences of individual variability.

ecology↗

GTP cyclohydrolase 1 and axanthism in ball pythons: a new vertebrate model for pterin-based pigmention

Pterin pigments are responsible for many of the bright colours observed across the animal kingdom. However, unlike melanin, the genetics of pterin-based pigmentation has received relatively little attention in animal colouration studies. Here, we investigate a lineage of axanthic ball pythons (Python regius) found in captivity as a model system to study pterin pigmentation in vertebrates. By crowdsourcing shed skin samples from commercial breeders and applying a case-control study design, we utilized whole-genome pool sequencing (pool-seq) and variant annotation. We identified a premature stop codon in the gene GTP cyclohydrolase II (gch2), which is associated with the axanthic phenotype. GCH2 catalyzes the first rate-limiting step in riboflavin biosynthesis. This study provides the first identification of an axanthism-associated gene in vertebrates and highlights the utility of ball pythons as a model to study pterin-based pigmentation.

genetics↗

Counter-gradient variation in gene expression between fish populations facilitates colonization of low-dissolved oxygen environments

The role of phenotypic plasticity during colonization remains unclear due to the shifting importance of plasticity across timescales. Over time, genetic responses can reduce plasticity such that species in a novel environment show higher levels of plasticity than those with a longer evolutionary timescale in the environment. Therefore, comparing species in the early stages of colonization to long-established species provides a powerful approach for uncovering the role of phenotypic plasticity during different stages of colonization. We compared gene expression between the cyprinid fish Enteromius apleurogramma, a species that has undergone a recent range expansion, and E. neumayeri, a long-established native species in the same region, caught from low-dissolved oxygen (DO) and high-DO habitats. We sampled tissue either immediately after capture from the field or after a two-week acclimation under high-DO conditions, allowing us to test for both evolved and plastic differences in low-DO vs high-DO populations of each species. We found that most genes showing evolved differences in gene expression did not overlap with those showing plastic differences in gene expression. However, in the genes that did overlap, there was counter-gradient variation such that plastic and evolved gene expression responses were in opposite directions in both species. Additionally, E. apleurogramma had higher levels of plasticity and evolved divergence in gene expression between field populations. We suggest that the higher level of plasticity and counter-gradient variation may have allowed rapid genetic adaptation in E. apleurogramma and facilitated colonization. This study shows how counter-gradient variation may impact colonization of divergent oxygen environments.

evolutionary biology↗

Dimensionality and modularity of adaptive variation: Divergence in threespine stickleback from diverse environments

In nature, populations are subjected to a wide variety of environmental conditions that affect fitness and induce adaptive or plastic responses in traits, resulting in phenotypic divergence between populations. The dimensionality of that divergence, however, remains contentious. At the extremes, some contend that populations diverge along a single axis of trait covariance with greatest availability of heritable variation, even if this does not lead a population directly to its fitness optimum. Those at the other extreme argue that selection can push populations towards their fitness optima along multiple phenotype axes simultaneously, resulting in divergence in numerous dimensions. Here, we address this debate using populations of threespine stickleback (Gasterosteus aculeatus) in the Cook Inlet region of southern Alaska from lakes with contrasting ecological conditions. We calculated effective dimensionality of divergence in several trait suites (defensive, swimming, and trophic) thought to be under correlated selection pressures, as well as across all traits. We also tested for integration among the trait suites and between each trait suite and the environment. We found that populations in the Cook Inlet radiation exhibit dimensionality of phenotype high enough to preclude a single axis of divergence.

evolutionary biology↗

The pace of modern life, revisited

Wild populations must continuously adapt to environmental changes or they risk extinction. Such adaptations can be measured as phenotypic rates of change and can allow us to predict patterns of contemporary evolutionary change. About two decades ago, a dataset of phenotypic rates of change in wild populations was compiled. Since then, researchers have used (and expanded) this dataset to look at microevolutionary processes in relation to specific types of human disturbances. Here, we have updated the dataset adding 5675 estimates of phenotypic changes and used it to revisit established patterns of contemporary evolutionary change. Using this newer version, containing 7338 estimates of phenotypic changes, we revisit the conclusions of four published articles. We then synthesize the expanded dataset to compare rates of change across different types of human disturbance. Analyses of this expanded dataset suggests that: I. a small absolute difference in rates of change exists between human disturbed and natural populations, II. harvesting by humans results in larger rates of change than other types of disturbances, III. introduced populations have increased rates of change, and IV. body size does not increase through time. Overall, findings from earlier analyses have largely held-up in analyses of our new dataset that encompass a much larger breadth of species, traits, and human disturbances. Lastly, we found that types of human disturbances affect rates of phenotypic change, and we call for this database to serve as a steppingstone for further analyses to understand patterns of contemporary evolution.

evolutionary biology↗

Using seasonal genomic changes to understand historical adaptation: parallel selection on stickleback in highly-variable estuaries

Parallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time. The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection in action under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing (Pool-WGS) to track seasonal allele frequency changes in these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.

genomics↗

Clinal genomic analysis reveals strong reproductive isolation across a steep habitat transition in stickleback fish

How ecological divergence causes strong reproductive isolation between populations in close geographic contact remains poorly understood at the genomic level. We here study this question in a stickleback population pair adapted to contiguous, ecologically different lake and stream habitats. Dense clinal whole-genome sequence data reveal numerous regions fixed for alternative alleles over a distance of just a few hundred meters. This strong polygenic adaptive divergence must constitute a genome-wide barrier to gene flow because a steep cline in allele frequencies is observed across the entire genome, and because the cline center co-localizes with the habitat transition. Simulations confirm that such strong reproductive isolation can be maintained by polygenic selection despite high dispersal and small per-locus selection coefficients. Finally, comparing samples from the cline center before and after an unusual ecological perturbation demonstrates the fragility of the balance between gene flow and selection. Overall, our study highlights the efficacy of divergent selection in maintaining reproductive isolation without physical isolation, and the analytical power of studying speciation at a fine eco-geographic and genomic scale.

evolutionary biology↗

Repeatability of adaptive radiation depends on spatial scale: regional versus global replicates of stickleback in lake versus stream habitats

The repeatability of adaptive radiation is expected to be scale dependent, with determinism decreasing as greater spatial separation among "replicates" leads to their increased genetic and ecological independence. Threespine stickleback (Gasterosteus aculeatus) provide an opportunity to test whether this expectation holds for the early stages of adaptive radiation - their diversification in freshwater ecosystems has been replicated many times. To better understand the repeatability of that adaptive radiation, we examined the influence of geographic scale on levels of parallel evolution by quantifying phenotypic and genetic divergence between lake and stream stickleback pairs sampled at regional (Vancouver Island) and global (North America and Europe) scales. We measured phenotypes known to show lake-stream divergence and used reduced representation genome-wide sequencing to estimate genetic divergence. We assessed the scale-dependence of parallel evolution by comparing effect sizes from multivariate models and also the direction and magnitude of lake-stream divergence vectors. At the phenotypic level, parallelism was greater at the regional than the global scale. At the genetic level, putative selected loci showed greater lake-stream parallelism at the regional than the global scale. Generally, the level of parallel evolution was low at both scales, except for some key univariate traits. Divergence vectors were often orthogonal, highlighting possible ecological and genetic constraints on parallel evolution at both scales. Overall, our results confirm that the repeatability of adaptive radiation decreases at increasing spatial scales. We suggest that greater environmental heterogeneity at larger scales imposes different selection regimes, thus generating lower repeatability of adaptive radiation at larger spatial scales.

evolutionary biology↗

Thirty-five experimental fisheries reveal the mechanisms of selection

Fisheries have been described as large-scale evolutionary experiments; yet such \"experiments\" tend to be poorly replicated and therefore lack the predictive power essential for designing appropriate management strategies to minimize the effects of fisheries-induced selection. Large-scale removal of non-native trout from 35 montane lakes in California provided repeated experimental fisheries that allowed us to explore how environmental parameters affect the three potential contributors to overall selection: the fitness-trait correlation, trait variability, and fitness variability. Our results demonstrate that fishing rapidly altered the size structure of harvested populations, and that the magnitude of change was primarily driven by the fitness-trait correlation (net selectivity). Fishing-induced selection was repeatable overall but was also influenced by environmental (lake size and quality) and demographic (size structure) parameters. Decomposing fishing-induced selection into its key components can improve the management of stocks experiencing fishing-induced selection by identifying the drivers of selection and therefore the appropriate target for management.

evolutionary biology↗