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Barrett, R. D. H.

Publications and source records attributed to Barrett, R. D. H..

11 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↗

Nutrient Enrichment and Connectivity Jointly Shape Bacterioplankton Diversity

It is increasingly important to understand the response of freshwater communities and ecosystems to fertilizers given their widespread usage and the propensity for these fertilizers to runoff into rivers and lakes. Dispersal, an important ecological factor mediated by landscape connectivity, could potentially counteract the impacts of anthropogenic stressors through the reintroduction of communities unperturbed by local stressors. However, this potential has not yet been studied in the context of nutrient stressed natural communities. Here, we investigate the impacts of nutrient enrichment and connectivity on freshwater bacterioplankton communities. We subjected mesocosms stocked with native bacterioplankton communities to different combinations of nutrient enrichment and connectivity (volumes of water transferred between mesocosms). We show that nutrient enrichment strongly structures the bacterioplankton community, favoring nutrient tolerant taxa and depressing taxonomic diversity. Connectivity, however, interacts with nutrient enrichment to restore functional diversity in communities subjected to the highest levels of nutrient stress. Despite the ameliorating effects of dispersal, nutrient enrichment leaves a consistent signature in communities, driving a shift from more heterotrophic to more phototrophic communities. Taken together, our results demonstrate that while nutrient enrichment significantly impacts freshwater bacterioplankton communities, connectivity can help restore functional diversity to a certain extent.

ecology↗

Genomics of freshwater adaptation in three-spine stickleback from eastern Canada

The threespine stickleback (Gasterosteus aculeatus) is a key model in evolutionary genetics, particularly for studies of parallel evolution, yet most genomic insights derive from populations on the west coast of North America and in Europe. Here, we use restriction site-associated DNA sequencing (RAD-seq) of pooled samples to examine genomic differentiation between marine and freshwater stickleback populations from Atlantic Canada. Our analyses reveal substantial heterogeneity in the extent and genomic distribution of marine-freshwater differentiation, with some freshwater populations showing strong divergence consistent with long-term isolation and drift, and others exhibiting patterns consistent with ongoing gene flow and admixture. Despite this demographic variation, we identify genomic regions that are repeatedly differentiated between marine and freshwater habitats, including loci near dopamine receptor genes (Drd4a and Drd2l). Gene ontology analyses of candidate regions show enrichment for functions related to nervous system development and dopamine receptor activity. Together, these results indicate that freshwater-associated genomic differentiation in Atlantic Canadian stickleback occurs across contrasting demographic contexts and suggest a potential role for neurological and behavioural pathways in adaptation to freshwater environments. Significance statementThreespine stickleback are a model system for studying parallel evolution, yet most genomic research has focused on Pacific and European populations. By examining previously understudied Atlantic Canadian populations, we identify genomic patterns consistent with parallel divergence across markedly heterogeneous demographic contexts, including populations shaped by strong drift as well as gene flow. We detect differentiation near dopamine receptor genes, pointing to a potential role for behavioural and hormonal pathways. Together, these results highlight the role of demographic context in shaping patterns of genomic differentiation associated with freshwater colonization.

genomics↗

Pre-exposure to stress reduces loss of community and genetic diversity following severe environmental disturbance

Environmental stress caused by anthropogenic impacts is increasing worldwide. Understanding the ecological and evolutionary consequences for biodiversity will be crucial for our ability to respond effectively. Historical exposure to environmental stress is expected to select for resistant species, shifting community composition towards more stress-tolerant taxa. Concurrent with this species sorting process, genotypes within resistant taxa that have the highest relative fitness under severe stress are expected to increase in frequency, leading to evolutionary adaptation. However, empirical demonstrations of these dual ecological and evolutionary processes in natural communities are lacking. Here, we provide the first evidence for simultaneous species sorting and evolutionary adaptation across multiple species within a natural freshwater bacterial community. Using a two-phase stressor experimental design (acidification pre-exposure followed by severe acidification) in aquatic mesocosms, we show that pre-exposed communities were more resistant than naive communities to taxonomic loss when faced with severe acid stress. However, after sustained severe acidification, taxonomic richness of both pre-exposed and naive communities eventually converged. All communities experiencing severe acidification became dominated by an acidophilic bacterium, Acidiphilium rubrum, but this species retained greater genetic diversity and followed distinct evolutionary trajectories in pre-exposed relative to naive communities. These patterns were shared across other acidophilic species, providing repeated evidence for the impact of pre-exposure on evolutionary outcomes despite the convergence of community profiles. Our results underscore the need to consider both ecological and evolutionary processes to accurately predict the responses of natural communities to environmental change.

evolutionary biology↗

A glyphosate-based herbicide selects for genetic changes while retaining within-species diversity in a freshwater bacterioplankton community

Bacterial populations evolve rapidly in the lab when faced with experimentally-applied selective pressures. Yet how bacteria evolve in nature, in more complex multi-species communities, is both challenging to study and essential to our understanding of ecosystem responses to rapid anthropogenic change. It has been theorized that selection purges within-species diversity in genome-wide selective sweeps, but the prevalence of such sweeps in response to known selective pressures in nature remains unclear. To track bacterial evolution in a semi-natural context, we applied Roundup, a glyphosate-based herbicide (GBH) as a selective pressure to 1000 L ponds containing bacterioplankton communities from a pristine lake. Using metagenomic analyses, we found that GBH treatment substantially affected community diversity, reducing species richness twofold, but did not consistently purge within-species genetic diversity over the four weeks of the experiment. We identified several functional categories of genes targeted by GBH selection across 11 different species of bacteria. There was no evidence for selection on the enzyme targeted by glyphosate, which interferes with amino acid synthesis; however genes involved more broadly in amino acid transport and metabolism were more likely to experience changes in allele frequency, particularly in inferred GBH-sensitive species. Together, these results show how environmental change can rapidly affect bacterial community structure while leaving within-species diversity largely intact. Even without evident genome-wide selective sweeps, we identify consistent genetic targets of selection, pointing to alternative mechanisms of GBH resistance in nature, and suggesting a role for soft or gene-specific selective sweeps in adaptation.

evolutionary biology↗

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↗

Heritability of DNA methylation in threespine stickleback (Gasterosteus aculeatus)

Epigenetic mechanisms underlying phenotypic change are hypothesized to contribute to population persistence and adaptation in the face of environmental change. To date, few studies have explored the heritability of intergenerationally stable methylation levels in natural populations, and little is known about the relative contribution of cis- and trans-regulatory changes to methylation variation. Here, we explore the heritability of DNA methylation, and conduct methylation quantitative trait loci (meQTL) analysis to investigate the genetic architecture underlying methylation variation between marine and freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We quantitatively measured genome-wide DNA methylation in fin tissue using reduced representation bisulfite sequencing of F1 and F2 crosses, and their marine and freshwater source populations. We identified cytosines (CpG sites) that exhibited stable methylation levels across generations. We found that genetic variance explained an average of 24 to 35% of the methylation variance, with a number of CpG sites possibly autonomous from genetic control. Finally, we detected both cis- and trans-meQTLs, with only trans-meQTLs overlapping with previously identified genomic regions of high differentiation between marine and freshwater ecotypes, as well as identified the genetic architecture underlying two key CpG sites that were differentially methylated between ecotypes. These findings demonstrate a potential role for DNA methylation in facilitating adaptation to divergent environments and improve our understanding of the heritable basis of population epigenomic variation.

evolutionary biology↗

Resistance, resilience, and functional redundancy of freshwater microbial communities facing multiple agricultural stressors in a mesocosm experiment

Agricultural pollution with fertilizers and pesticides is a common disturbance to freshwater biodiversity. Bacterioplankton communities are at the base of aquatic food webs, but their responses to these potentially interacting stressors are rarely explored. To test the extent of resistance and resilience in bacterioplankton communities faced with agricultural stressors, we exposed freshwater mesocosms to single and combined gradients of two commonly used pesticides: the herbicide glyphosate (0-15 mg/L) and the neonicotinoid insecticide imidacloprid (0-60 g/L), in high or low nutrient backgrounds. Over the 43-day experiment, we tracked variation in bacterial density with flow cytometry, carbon substrate use with Biolog EcoPlates, and taxonomic diversity and composition with environmental 16S rRNA gene amplicon sequencing. We show that only glyphosate (at the highest dose, 15 mg/L), but not imidacloprid, nutrients, or their interactions measurably changed community structure, favoring members of the Proteobacteria including the genus Agrobacterium. However, no change in carbon substrate use was detected throughout, suggesting functional redundancy despite taxonomic changes. We further show that communities are resilient at broad, but not fine taxonomic levels: 24 days after glyphosate application the precise amplicon sequence variants do not return, and tend to be replaced by phylogenetically close taxa. We conclude that high doses of glyphosate - but still within commonly acceptable regulatory guidelines - alter freshwater bacterioplankton by favoring a subset of higher taxonomic units (i.e. genus to phylum) that transiently thrive in the presence of glyphosate. Longer-term impacts of glyphosate at finer taxonomic resolution merit further investigation.

ecology↗

Community rescue in experimental phytoplankton communities facing severe herbicide pollution.

Evolutionary rescue occurs when adaptation prevents local extinction in deteriorating environments. Laboratory experiments with microorganisms have shown that the likelihood of evolutionary rescue is greatest in large populations that have previously experienced sublethal doses of stress. To assess this result in natural communities, we conducted a mesocosm experiment with semi-natural phytoplankton communities exposed to glyphosate, a widely used herbicide. We tested whether community biomass and pre-exposure to sublethal stress would facilitate community rescue after severe contamination. Exposure to sublethal stress, but not community biomass, facilitated rescue significantly-even though it led to biodiversity loss. Furthermore, glyphosate had modest effects on community composition, suggesting that community resistance to glyphosate was primarily driven by changes in resistance within taxa, not by community turnover. Our results expand the scope of community evolutionary rescue theory to complex ecosystems and confirm that prior stress exposure is a key predictor of rescue.

ecology↗

The fitness consequences of genetic variation in wild populations of mice

Adaptive evolution can occur when genetic change affects traits subject to natural selection. Although selection is a deterministic process, adaptation can be difficult to predict in finite populations because the functional connections between genotype, phenotype, and fitness are complex. Here, we make these connections using a combination of field and laboratory experiments. We conduct a large-scale manipulative field experiment with wild populations of deer mice in distinct habitats to directly estimate natural selection on pigmentation traits and next test whether this selection drives changes in allele frequency at an underlying pigment locus. We find that divergent cryptic phenotypes are repeatedly favoured in each habitat, leaving footprints of selection in the Agouti gene. Next, using transgenic experiments in Mus, we functionally test one of the Agouti mutations associated with survival, a Serine deletion in exon 2, and find that it causes lighter coat colour via changes in its protein binding properties. Finally, we show significant change in the frequency of this mutation in our field experiment. Together, our findings demonstrate how a sequence variant alters phenotype and show the ensuing ecological consequences that drive changes in population allele frequency, thereby revealing the full process of evolution by natural selection.

evolutionary biology↗