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Rudman, S. M.

Publications and source records attributed to Rudman, S. M..

14 recordsLinked to original sources

Insecticide resistance evolution and assisted gene flow interact to shape the evolution of plasticity

Adaptive phenotypic plasticity can bolster fitness in changing environments, but the extent to which plasticity evolves rapidly, and which forces shape this evolutionary trajectory, is largely unknown. To empirically study the evolution of plasticity we first conducted a replicated field experiment in which Drosophila melanogaster populations adapted to insecticide exposure and a subset of these populations received high diversity assisted gene flow. We then reared individuals from each population across temperature and insecticide treatments in common garden to test the following questions: 1. Has prior selection and rapid adaptation of insecticide resistance led to evolved shifts in plasticity relative to naive populations? 2. Does gene flow from genetically diverse populations contribute to adaptive plasticity evolution relative to gene flow-restricted low diversity populations? Both gene flow and prior evolution of resistance influenced the evolution of plasticity for multiple traits and were often maladaptive for resistant and gene flow-restricted populations, suggesting a trade-off between trait and plasticity evolution. Assisted gene flow minimized maladaptive plasticity potentially through relaxation of underlying epistatic or pleiotropic constraints. Together, these results demonstrate the dynamic interactions between trait evolution, the evolution of plasticity, and forces that shape genetic diversity with implications for conservation of threatened populations.

evolutionary biology↗

Ecological stoichiometry and life history theory, not the identity of genomic variants, predict rapid adaptation

SignificanceForecasting how populations adapt to changing environments is a central challenge in evolutionary biology. We tested the predictability of rapid adaptation by tracking both phenotypic and genomic trajectories of evolution in replicate outdoor populations of Drosophila melanogaster and comparing these data to predictions derived from life history theory, ecological stoichiometry, and genomic data. We found that life history theory and ecological stoichiometry forecasted the direction of phenotypic evolution, even with temporal changes in the direction of evolution. In contrast, genomic predictors were largely unable to forecast the SNPs or genes underlying adaptation. These results demonstrate the utility of ecological frameworks to provide general, but robust, forecasts of adaptation in complex environments. Determining the scale and scope of the predictability of evolution is fundamental to understanding biological processes and to managing biodiversity. Ecological frameworks, including life history theory and ecological stoichiometry, offer testable predictions about the direction of adaptation and trade-offs between traits in response to environmental change. Similarly, well-characterized molecular pathways, genotype-phenotype linkages, and prior evolutionary genomic studies could be predictive of the genomic architecture underlying adaptation. We tested whether ecological frameworks and evolutionary genomic data can be used to forecast rapid adaptation in replicated outdoor populations of Drosophila melanogaster evolving in response to natural seasonal fluctuations from summer to late fall. Life history theory predicted the observed pattern of adaptive tracking: in summer, reproductive output increased and stress tolerance decreased, while in fall, this direction reversed, with evolution of increased stress tolerance at the expense of reproduction. Stoichiometric phenotypic evolution was also predictable, with phosphorus and magnesium content, both linked to growth rate, and alkali metal, associated with maintaining homeostasis in response to thermal stress, showing rapid and parallel evolution indicative of adaptation. Temporal genomic data revealed a complex genomic architecture of temporal adaptation and the SNPs and genes involved in adaptation were largely unpredictable. These results demonstrate that ecological frameworks, more than genomic data, have utility in forecasting adaptation in complex and variable environments.

evolutionary biology↗

Seasonal evolution of Drosophila melanogaster abdominal pigmentation is associated with a multifarious selective landscape

Pigmentation has been widely studied by evolutionary biologists due to both ease of measure and relationship to fitness. Drosophila melanogaster pigmentation has represented a particularly useful avenue of investigation, as extensive genetic tools have enabled the characterization of the traits complex architecture. Drosophila pigmentation also varies predictably across space and time in wild populations, suggesting pigmentation is a component of adaptation to local environmental conditions. Despite this, the impact of D. melanogaster pigmentation on fitness, and the environmental factors that drive the evolution of pigmentation, are not well understood. To address this gap, we experimentally evolved replicated D. melanogaster populations in field mesocosms to determine whether and how pigmentation evolves in response to environmental variation. We found that pigmentation rapidly and predictably adapted to a direct manipulation of temperature, supportive of melanization playing a role in thermoregulation. However, we also determined that pigmentation responded adaptively to direct manipulations of numerous additional factors, including intraspecific competition, diet, and the microbiome. These findings suggest that the selective landscape acting on pigmentation is complex and multifaceted, and that patterns of melanization may be driven, at least in part, by indirect selection due to correlations with other fitness-related traits.

evolutionary biology↗

Microbiome evolution plays a secondary role in host rapid adaptation

Understanding how populations adapt to environmental change is a central goal in evolutionary biology. Microbiomes have been proposed as a source of heritable variation that is central to rapid adaptation in hosts, yet empirical evidence supporting this remains limited, particularly in naturalistic settings. We combined a field evolution experiment in Drosophila melanogaster exposed to an insecticide with microbiome manipulations to disentangle the contributions of host standing genetic variation and microbiome evolution to adaptation. Within three generations, independent populations rapidly and repeatedly evolved increased survivorship, a defining feature of resistance evolution. Adaptive changes in sub-lethal traits such as reproductive output, stress tolerance, and body size occurred with a delayed response following the evolution of resistance. Core microbiome taxa declined following insecticide exposure, and resistant populations evolved to house lower microbial abundances. Axenic rearing and microbiome transplant experiments demonstrated that adaptation via host standing genetic variation was the mechanism for resistance evolution. Microbiome evolution played a secondary and cryptic role in host adaptation by masking slowed development rates that evolved in resistant populations. Together, these results reinforce the primacy of adaptation occurring through selection on host standing genetic variation while also demonstrating the contributions of microbiome evolution in host adaptation. SignificanceIdentifying the mechanisms that allow organisms to adapt to environmental stress is a foundational goal in biology. Using field experimental evolution and microbiome manipulations in Drosophila melanogaster, we directly tested the relative contributions of host genomic evolution and microbiome evolution to adaptation. We found that adaptation to environmental stress occurred rapidly and repeatedly, driven primarily by selection on host standing genetic variation, with microbiome evolution acting as a secondary contributor. These findings reinforce the importance of host genetic variation in rapid adaptation and demonstrate that microbiome evolution can contribute to host evolutionary trajectories in a cryptic manner.

evolutionary biology↗

Adaptation and trade-offs with insecticide resistance in overwintering Drosophila

Winter is a formidable challenge for ectotherms that inhabit temperate climates. Prior work has demonstrated that multivoltine organisms can evolve rapidly in response to temporal changes within a growing season, a process termed adaptive tracking. However, the mechanisms by which winter conditions drive rapid adaptation, particularly when combined with strong anthropogenic stressors, remain poorly understood. Here we use replicate populations of Drosophila melanogaster in a field experiment to test i) whether winter conditions drive rapid adaptation and ii) for trade-offs between insecticide resistance and overwintering survival. Following a longitudinal field experiment spanning summer and fall investigating the evolution of insecticide resistance, we tracked subsequent evolution during an overwintering period. We detected repeated evolutionary shifts indicative of adaptation to winter conditions in multiple traits, including body size and fecundity. Additionally, populations that had evolved insecticide resistance during the growing season had reduced survival and showed patterns of lower resistance following the winter period, suggestive of a trade-off between overwintering success and insecticide resistance. These rapid evolutionary responses and potential trade-offs provide important context for understanding overwintering performance in temperate insects, with implications for pest management and ecosystem services.

evolutionary biology↗

A test for microbiome-mediated rescue via host phenotypic plasticity in Daphnia

Phenotypic plasticity is a primary mechanism by which organismal phenotypes shift in response to the environment. Host-associated microbiomes often exhibit considerable shifts in response to environmental variation and these shifts could facilitate host phenotypic plasticity, adaptation, or rescue populations from extinction. However, it is unclear how much shifts in microbiome composition contribute to host phenotypic plasticity, limiting our knowledge of the underlying mechanisms of plasticity and, ultimately, the fate of populations inhabiting changing environments. In this study, we examined phenotypic responses and microbiome composition in 20 genetically distinct Daphnia magna clones exposed to non-toxic and toxic diets containing Microcystis, a cosmopolitan cyanobacteria and common stressor for Daphnia. Daphnia exhibited significant plasticity in survival, reproduction, and population growth rates in response to Microcystis exposure. However, the effects of Microcystis exposure on the Daphnia microbiome were limited, with the primary effect being differences in abundance observed across five bacterial families. Moreover, there was no significant correlation between the magnitude of microbiome shifts and host phenotypic plasticity. Our results suggest that microbiome composition played a negligible role in driving host phenotypic plasticity or microbiome-mediated rescue. One sentence summaryDaphnia exhibits considerable plasticity in individual and population-level responses to a cosmopolitan stressor, yet shifts in microbiome composition are not correlated with the magnitude of this plasticity.

ecology↗

Transgenerational epigenetic inheritance increases trait variation but is not adaptive

Understanding processes that can produce adaptive phenotypic shifts in response to rapid environmental change is critical to reducing biodiversity loss. The ubiquity of environmentally induced epigenetic marks has led to speculation that epigenetic inheritance could potentially enhance population persistence in response to environmental change. Yet, the magnitude and fitness consequences of epigenetic marks carried beyond maternal inheritance are largely unknown. Here, we tested how transgenerational epigenetic inheritance (TEI) shapes the phenotypic response of Daphnia clones to the environmental stressor Microcystis. We split individuals from each of eight genotypes into exposure and control treatments (F0 generation) and tracked the fitness of their descendants to the F3 generation. We found transgenerational epigenetic exposure to Microcystis led to reduced rates of survival and individual growth and no consistent effect on offspring production. Increase in trait variance in the F3 relative to F0 generations suggests potential for heritable bet hedging driven by TEI, which could impact population dynamics. Our findings are counter to the working hypothesis that TEI is a generally adaptive mechanism likely to prevent extinction for populations inhabiting rapidly changing environments. One sentence summaryTransgenerational epigenetic inheritance in Daphnia exposed to Microcystis revealed negative fitness effects on survival and growth rates, challenging hypotheses of a general selective advantage.

evolutionary biology↗

MLDAAPP: Machine Learning Data Acquisition for Assessing Population Phenotypes

Collecting phenotypic data from many individuals is critical to numerous biological disciplines. Yet, organismal phenotypic or trait data are still often collected manually, limiting the scale of data collection, precluding reproducible workflows, and creating the potential for human bias. Computer vision could largely ameliorate these issues, but currently available packages only operate with specific inputs and hence are not scalable or accessible for many biologists. We present Machine Learning Data Acquisition for Assessing Population Phenotypes (MLDAAPP), a package of tools for collecting phenotypic data from groups of individuals. We demonstrate that MLDAAPP is both accurate and uniquely effective at measuring phenotypes in challenging conditions - particularly images and videos of varying quality derived from both lab and field environments. Employing MLDAAPP solves key issues of reproducibility, increases both the scale and scope of data generation, and reduces the potential for human bias.

evolutionary biology↗

Intraspecific genetic variation is critical to robust toxicological predictions in Daphnia

Environmental risk assessment is a critical tool for protecting aquatic life and its effectiveness is predicated on predicting how natural populations respond to contaminants. Yet, routine toxicity testing typically examines only one genotype, which may render risk assessments inaccurate as populations are most often composed of genetically distinct individuals. To determine the importance of intraspecific variation in the translation of toxicity testing to populations, we quantified the magnitude of genetic variation within 20 Daphnia magna clones derived from one lake using whole genome sequencing and phenotypic assays. We repeated these assays across two exposure levels of microcystins, a cosmopolitan and lethal aquatic contaminant produced by harmful algal blooms. We found considerable intraspecific genetic variation in survival, growth, and reproduction, which was amplified by microcystins exposure. Finally, using simulations we demonstrate that the common practice of employing a single genotype to calculate toxicity tolerance failed to produce an estimate within the 95% confidence interval over half of the time. These results illuminate the importance of incorporating intraspecific genetic variation into toxicity testing to reliably predict how natural populations will respond to aquatic contaminants.

pharmacology and toxicology↗

Low human health risks of algal toxins from consuming fish caught in Lake St. Clair

Consuming fish exposed to cyanobacterial harmful algal blooms (HABs) may be a major route of microcystin toxin exposure to humans. However, it remains unknown whether fish can accumulate and retain microcystins temporally in waterbodies with recurring seasonal HABs, particularly before and after a HAB event when fishing is active. We conducted a field study on Largemouth Bass, Northern Pike, Smallmouth Bass, Rock Bass, Walleye, White Bass, and Yellow Perch to assess the human health risks to microcystin toxicity via fish consumption. We collected 124 fish in 2016 and 2018 from Lake St. Clair, a large freshwater ecosystem in the North American Great Lakes that is actively fished pre- and post-HAB periods. Muscles were analyzed using the MMPB Lemieux Oxidation method for total microcystins, which was used to perform a human health risk assessment for comparison against fish consumption advisory benchmarks available for Lake St. Clair. From this collection 35 fish livers were additionally extracted to confirm the presence of microcystins. Microcystins were detected in all livers at widely varying concentrations (1-1,500 ng g-1 ww), suggesting HABs are an underappreciated and pervasive stressor to fish populations. Conversely, microcystin levels were consistently low in muscles (0-15 ng g-1 ww) and presented negligible risk, empirically supporting that fillets may be safely consumed before and after HAB events following fish consumption advisories.

ecology↗

Elemental stoichiometry and insect chill tolerance: Evolved and plastic changes in organismal Na+ and K+ content in Drosophila

Acclimation and evolutionary adaptation can produce phenotypic change that allows organisms to cope with challenges like those associated with climate change. Determining the relative contributions of acclimation and adaptation is of central importance to understanding animal responses to change. Rates of evolution have traditionally been considered slow relative to ecological processes that shape biodiversity. Many organisms nonetheless show patterns of spatial genetic variation suggestive of adaptation and some evidence is emerging that adaptation can act sufficiently fast to allow phenotypic tracking in response to environmental change ( adaptive tracking). In Drosophila, both plastic and evolved differences in chill tolerance are associated with ionoregulation. Here we combine acclimation, latitudinal field collections, and a replicated field experiment to assess the effects of acclimation and adaptation on chill coma recovery and elemental (Na and K) stoichiometry in both sexes of Drosophila melanogaster. Acclimation and spatial adaptation both shape chill coma recovery, with acclimation producing the greatest magnitude response. Leveraging knowledge on the physiological mechanisms that underlie variation in chill tolerance traits, we find that the relationship between K content and chill tolerance differs among flies acclimated vs. adapted to cold. Taken together, these data reinforce the importance of acclimation in responses to abiotic challenges and illustrate that the mechanisms of phenotypic change can differ between acclimation and basal tolerance adaptation.

evolutionary biology↗

Lake Erie fish safe to eat yet afflicted by algal hepatotoxins

Microcystin toxins from harmful algal blooms (HABs) can accumulate and persist in fish, raising dual concerns about human health risks from consumption and the potential for detrimental impacts on fish populations. However, there are fundamental unknowns about the relationship between HABs and fish populations driven by a lack of field information on toxin accumulation and retention over space and time. We conducted a field study to assess human health risks from consuming fish caught across all life stages of a HAB and to determine the pervasiveness of potentially harmful levels of microcystins on fish populations. We collected 190 fish in 2015 and 2017 from Lake Erie, a large freshwater ecosystem that is highly productive for fisheries and is an epicenter of HABs and microcystin toxicity events. Muscles and livers were analyzed for total microcystins, which was used to conduct a human health risk assessment for comparison against fish consumption advisory benchmarks available for Lake Erie. We find low human health risk from muscle consumption following the World Health Organizations safety thresholds. However, all fish across capture dates had microcystins in their livers at levels shown to cause adverse effects, suggesting a pervasive and underappreciated toxic stressor. These data demonstrate that microcystins are retained in fish livers well beyond the cessation of HABs and calls for additional research to better understand the effects of sublethal toxic exposures for fish population dynamics, conservation, and related ecosystem services.

ecology↗

Direct observation of adaptive tracking on ecological timescales in Drosophila

Direct observation of evolution in response to natural environmental change can resolve fundamental questions about adaptation including its pace, temporal dynamics, and underlying phenotypic and genomic architecture. We tracked evolution of fitness-associated phenotypes and allele frequencies genome-wide in ten replicate field populations of Drosophila melanogaster over ten generations from summer to late fall. Adaptation was evident over each sampling interval (1-4 generations) with exceptionally rapid phenotypic adaptation and large allele frequency shifts at many independent loci. The direction and basis of the adaptive response shifted repeatedly over time, consistent with the action of strong and rapidly fluctuating selection. Overall, we find clear phenotypic and genomic evidence of adaptive tracking occurring contemporaneously with environmental change, demonstrating the temporally dynamic nature of adaptation. One sentence summaryRapid environmental change drives continuous phenotypic and polygenic adaptation, demonstrating the temporal dynamism of adaptation.

evolutionary biology↗

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↗