Search USGSSearch

Geology topics

Brenna R. Forester

Publications and source records attributed to Brenna R. Forester.

11 recordsLinked to original sources

Population genomics reveals local adaptation related to temperature variation in two stream frog species: Implications for vulnerability to climate warming

Identifying populations at highest risk from climate change is a critical component of conservation efforts. However, vulnerability assessments are usually applied at the species level, even though intraspecific variation in exposure, sensitivity and adaptive capacity play a crucial role in determining vulnerability. Genomic data can inform intraspecific vulnerability by identifying signatures of local adaptation that reflect population-level variation in sensitivity and adaptive capacity. Here, we address the question of local adaptation to temperature and the genetic basis of thermal tolerance in two stream frogs ( Ascaphus truei and A. montanus ). Building on previous physiological and temperature data, we used whole-genome resequencing of tadpoles from four sites spanning temperature gradients in each species to test for signatures of local adaptation. To support these analyses, we developed the first annotated reference genome for A. truei . We then expanded the geographic scope of our analysis using targeted capture at an additional 11 sites per species. We found evidence of local adaptation to temperature based on physiological and genomic data in A. montanus and genomic data in A. truei , suggesting similar levels of sensitivity (i.e., susceptibility) among populations regardless of stream temperature. However, invariant thermal tolerances across temperatures in A. truei suggest that populations occupying warmer streams may be most sensitive. We identified high levels of evolutionary potential in both species based on genomic and physiological data. While further integration of these data is needed to comprehensively evaluate spatial variation in vulnerability, this work illustrates the value of genomics in identifying spatial patterns of climate change vulnerability.

Idaho, Montana, Oregon, Washington

Greater plasticity in CTmax with increased climate variability among populations of tailed frogs

Temporally variable climates are expected to drive the evolution of thermal physiological traits that enable performance across a wider range of temperatures (i.e. climate variability hypothesis, CVH). Spatial thermal variability, however, may mediate this relationship by providing ectotherms with the opportunity to behaviourally select preferred temperatures (i.e. the Bogert effect). These antagonistic forces on thermal physiological traits may explain the mixed support for the CVH within species despite strong support among species at larger geographical scales. Here, we test the CVH as it relates to plasticity in physiological upper thermal limits (critical thermal maximum—CTmax) among populations of coastal tailed frogs ( Ascaphus truei ). We targeted populations that inhabit spatially homogeneous environments, reducing the potentially confounding effects of behavioural thermoregulation. We found that populations experiencing greater temporal thermal variability exhibited greater plasticity in CTmax, supporting the CVH. Interestingly, we identified only one site with spatial temperature variability and tadpoles from this site demonstrated greater plasticity than expected, suggesting the opportunity for behavioural thermoregulation can reduce support for the CVH. Overall, our results demonstrate one role of climate variability in shaping thermal plasticity among populations and provide a baseline understanding of the impact of the CVH in spatially homogeneous thermal landscapes.

Proceedings of the Royal Society B

DNA-based studies and genetic diversity indicator assessments are complementary approaches to conserving evolutionary potential

Genetic diversity is essential for maintaining healthy populations and ecosystems. Several approaches have recently been developed to evaluate population genetic trends without necessarily collecting new genetic data. Such “genetic diversity indicators” enable rapid, large-scale evaluation across dozens to thousands of species. Empirical genetic studies, when available, provide detailed information that is important for management, such as estimates of gene flow, inbreeding, genetic erosion and adaptation. In this article, we argue that the development and advancement of genetic diversity indicators is a complementary approach to genetic studies in conservation biology, but not a substitute. Genetic diversity indicators and empirical genetic data can provide different information for conserving genetic diversity. Genetic diversity indicators enable affordable tracking, reporting, prioritization and communication, although, being proxies, do not provide comprehensive evaluation of the genetic status of a species. Conversely, genetic methods offer detailed analysis of the genetic status of a given species or population, although they remain challenging to implement for most species globally, given current capacity and resourcing. We conclude that indicators and genetic studies are both important for genetic conservation actions and recommend they be used in combination for conserving and monitoring genetic diversity.

Conservation Genetics

Multinational evaluation of genetic diversity indicators for the Kunming-Montreal Global Biodiversity Framework

Under the recently adopted Kunming-Montreal Global Biodiversity Framework, 196 Parties committed to reporting the status of genetic diversity for all species. To facilitate reporting, three genetic diversity indicators were developed, two of which focus on processes contributing to genetic diversity conservation: maintaining genetically distinct populations and ensuring populations are large enough to maintain genetic diversity. The major advantage of these indicators is that they can be estimated with or without DNA-based data. However, demonstrating their feasibility requires addressing the methodological challenges of using data gathered from diverse sources, across diverse taxonomic groups, and for countries of varying socio-economic status and biodiversity levels. Here, we assess the genetic indicators for 919 taxa, representing 5271 populations across nine countries, including megadiverse countries and developing economies. Eighty-three percent of the taxa assessed had data available to calculate at least one indicator. Our results show that although the majority of species maintain most populations, 58% of species have populations too small to maintain genetic diversity. Moreover, genetic indicator values suggest that IUCN Red List status and other initiatives fail to assess genetic status, highlighting the critical importance of genetic indicators.

Ecology Letters

Acclimation capacity of critical thermal maximum varies among populations: Consequences for estimates of vulnerability

Adaptive plasticity in thermal tolerance traits may buffer organisms against changing temperatures, making such responses of particular interest in the face of global climate change. Although population variation is integral to the evolvability of this trait, many studies inferring proxies of physiological vulnerability from thermal tolerance traits extrapolate data from one or a few populations to represent the species. Estimates of physiological vulnerability can be further complicated by methodological effects associated with experimental design. We evaluated how populations varied in their acclimation capacity (i.e., the magnitude of plasticity) for critical thermal maximum (CTmax) in two species of tailed frogs (Ascaphidae), cold-stream specialists. We used the estimates of acclimation capacity to infer physiological vulnerability to future warming. We performed CTmax experiments on tadpoles from 14 populations using a fully factorial experimental design of two holding temperatures (8 and 15°C) and two experimental starting temperatures (8 and 15°C). This design allowed us to investigate the acute effects of transferring organisms from one holding temperature to a different experimental starting temperature, as well as fully acclimated responses by using the same holding and starting temperature. We found that most populations exhibited beneficial acclimation, where CTmax was higher in tadpoles held at a warmer temperature, but populations varied markedly in the magnitude of the response and the inferred physiological vulnerability to future warming. We also found that the response of transferring organisms to different starting temperatures varied substantially among populations, although accounting for acute effects did not greatly alter estimates of physiological vulnerability at the species level or for most populations. These results underscore the importance of sampling widely among populations when inferring physiological vulnerability, as population variation in acclimation capacity and thermal sensitivity may be critical when assessing vulnerability to future warming.

Montana, Oregon

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Wildlife diseases are a major global threat to biodiversity. Boreal toads ( Anaxyrus [Bufo] boreas ) are a state-endangered species in the southern Rocky Mountains of Colorado and New Mexico, and a species of concern in Wyoming, largely due to lethal skin infections caused by the amphibian chytrid fungus Batrachochytrium dendrobatidis ( Bd ). We performed conservation and landscape genomic analyses using single nucleotide polymorphisms from double-digest, restriction site-associated DNA sequencing in combination with the development of the first boreal toad (and first North American toad) reference genome to investigate population structure, genomic diversity, landscape connectivity and adaptive divergence. Genomic diversity ( π = 0.00034–0.00040) and effective population sizes ( N e = 8.9–38.4) were low, likely due to post-Pleistocene founder effects and Bd -related population crashes over the last three decades. Population structure was also low, likely due to formerly high connectivity among a higher density of geographically proximate populations. Boreal toad gene flow was facilitated by low precipitation, cold minimum temperatures, less tree canopy, low heat load and less urbanization. We found >8X more putatively adaptive loci related to Bd intensity than to all other environmental factors combined, and evidence for genes under selection related to immune response, heart development and regulation and skin function. These data suggest boreal toads in habitats with Bd have experienced stronger selection pressure from disease than from other, broad-scale environmental variations. These findings can be used by managers to conserve and recover the species through actions including reintroduction and supplementation of populations that have declined due to Bd .

Colorado

Multi-scale relationships in thermal limits within and between two cold-water frog species uncover different trends in physiological vulnerability

1. Critical thermal limits represent an important component of an organism's capacity to cope with future temperature changes. Understanding the drivers of variation in these traits may uncover patterns in physiological vulnerability to climate change. Local temperature extremes have emerged as a major driver of thermal limits, although their effects can be mediated by the exploitation of fine-scale spatial variation in temperature through behavioural thermoregulation. 2. Here, we investigated thermal limits along elevation gradients within and between two cold-water frog species ( Ascaphus spp.), one with a coastal distribution ( A. truei ) and the other with a continental range ( A. montanus ). We quantified thermal limits for over 700 tadpoles, representing multiple populations from each species. We combined local temporal and fine-scale spatial temperature data to quantify local thermal landscapes (i.e., thermalscapes), including the opportunity for behavioural thermoregulation. 3. Lower thermal limits for either species could not be reached experimentally without the water freezing, suggesting that cold tolerance is <0.3°C. By contrast, upper thermal limits varied among populations, but this variation only reflected local temperature extremes in A . montanus , perhaps as a consequence of the greater variation in stream temperatures across its range. Lastly, we found minimal fine-scale spatial variability in temperature, suggesting limited opportunity for behavioural thermoregulation and thus increased vulnerability to warming for all populations. 4. By quantifying local thermalscapes, we uncovered different trends in the relative vulnerability of populations across elevation for each species. In A . truei , physiological vulnerability decreased with elevation, whereas in A . montanus , all populations were equally physiologically vulnerable. These results highlight how similar environments can differentially shape physiological tolerance and patterns of vulnerability of species, and in turn impact their vulnerability to future warming.

Montana

Genomics-informed delineation of conservation units in a desert amphibian

Delineating conservation units (CUs, e.g., evolutionarily significant units, ESUs, and management units, MUs) is critical to the recovery of declining species because CUs inform both listing status and management actions. Genomic data have strengths and limitations in informing CU delineation and related management questions in natural systems. We illustrate the value of using genomic data in combination with landscape, dispersal, and occupancy data, to inform CU delineation in Nevada populations of the Great Basin Distinct Population Segment of the Columbia spotted frog ( Rana luteiventris ). R. luteiventris occupies naturally fragmented aquatic habitats in this xeric region, but beaver removal, climate change, and other factors have put many of these populations at high risk of extirpation without management intervention. We addressed three objectives: (1) assessing support for ESUs within Nevada; (2) evaluating and revising, if warranted, the current delineation of MUs; and (3) evaluating genetic diversity, effective population size, adaptive differentiation, and functional connectivity to inform ongoing management actions. We found little support for ESUs within Nevada but did identify potential revisions to MUs based on unique landscape drivers of connectivity that distinguish these desert populations from those in the northern portion of the species range. Effective sizes were uniformly small, with low genetic diversity and weak signatures of adaptive differentiation. Our findings suggest that management actions, including translocations and genetic rescue, might be warranted. Our study illustrates how a carefully planned genetic study, designed to address priority management goals that include CU delineation, can provide multiple insights to inform conservation action.

Molecular Ecology

Linking evolutionary potential to extinction risk: Applications and future directions

Extinction-risk assessments play a major role in prioritizing conservation action at national and international levels. However, quantifying extinction risk is challenging, especially when including the full suite of adaptive responses to environmental change. In particular, evolutionary potential (EP), the capacity to evolve genetically based changes that increase fitness under changing conditions, has proven difficult to evaluate, limiting its inclusion in risk assessments. Theory, experiments, simulations, and field studies all highlight the importance of EP in characterizing and mitigating extinction risk. Disregarding EP can therefore result in ineffective allocation of resources and inadequate recovery planning. Fortunately, proxies for EP can be estimated from environmental, phenotypic, and genetic data. Some proxies can be incorporated into quantitative extinction-risk assessments, whereas others better inform basic conservation actions that maximize resilience to future change. Integration of EP into conservation decision-making is challenging but essential and remains an important area for innovation in applied conservation science.

Frontiers in Ecology and the Environment

Genomic signatures of thermal adaptation are associated with clinal shifts of life history in a broadly distributed frog

Temperature is a critical driver of ectotherm life-history strategies, whereby a warmer environment is associated with increased growth, reduced longevity and accelerated senescence. Increasing evidence indicates that thermal adaptation may underlie such life-history shifts in wild populations. Single nucleotide polymorphisms (SNPs) and copy number variants (CNVs) can help uncover the molecular mechanisms of temperature-driven variation in growth, longevity and senescence. However, our understanding of these mechanisms is still limited, which reduces our ability to predict the response of non-model ectotherms to global temperature change. In this study, we examined the potential role of thermal adaptation in clinal shifts of life-history traits (i.e. life span, senescence rate and recruitment) in the Columbia spotted frog Rana luteiventris along a broad temperature gradient in the western United States. We took advantage of extensive capture–recapture datasets of 20,033 marked individuals from eight populations surveyed annually for 14–18 years to examine how mean annual temperature and precipitation influenced demographic parameters (i.e. adult survival, life span, senescence rate, recruitment and population growth). After showing that temperature was the main climatic predictor influencing demography, we used RAD-seq data (50,829 SNPs and 6,599 putative CNVs) generated for 352 individuals from 31 breeding sites to identify the genomic signatures of thermal adaptation. Our results showed that temperature was negatively associated with annual adult survival and reproductive life span and positively associated with senescence rate. By contrast, recruitment increased with temperature, promoting the long-term viability of most populations. These temperature-dependent demographic changes were associated with strong genomic signatures of thermal adaptation. We identified 148 SNP candidates associated with temperature including three SNPs located within protein-coding genes regulating resistance to cold and hypoxia, immunity and reproduction in ranids. We also identified 39 CNV candidates (including within 38 transposable elements) for which normalized read depth was associated with temperature. Our study indicates that both SNPs and structural variants are associated with temperature and could eventually be found to play a functional role in clinal shifts in senescence rate and life-history strategies in R. luteiventris . These results highlight the potential role of different sources of molecular variation in the response of ectotherms to environmental temperature variation in the context of global warming.

Journal of Animal Ecology

Improving conservation policy with genomics: A guide to integrating adaptive potential into U.S. Endangered Species Act decisions for conservation practitioners and geneticists

Rapid environmental change makes adaptive potential—the capacity of populations to evolve genetically based changes in response to selection—more important than ever for long-term persistence of at-risk species. At the same time, advances in genomics provide unprecedented power to test for and quantify adaptive potential, enabling consideration of adaptive potential in estimates of extinction risk and laws protecting endangered species. The U.S. Endangered Species Act (ESA) is one of the most powerful environmental laws in the world, but so far, the full potential of genomics in ESA listing and recovery decisions has not been realized by the federal agencies responsible for implementing the ESA or by conservation geneticists. The goal of our paper is to chart a path forward for integrating genomics into ESA decision making to facilitate full consideration of adaptive potential in evaluating long-term risk of extinction. For policy makers, managers, and other conservation practitioners, we outline why adaptive potential is important for population persistence and what genomic tools are available for quantifying it. For conservation geneticists, we discuss how federal agencies can integrate information on the effect of adaptive potential on extinction risk—and the related uncertainty—into decisions, and suggest next steps for advancing understanding of the effect of adaptive potential on extinction risk. The mechanisms and consequences of adaptation are incredibly complex, and we may never have a complete understanding of adaptive potential for any organism. Nevertheless, we argue that the best available evidence regarding adaptive potential should be incorporated by federal agencies into modeling and decision making processes now, while at the same time conserving genome-wide variation and striving for a deeper understanding of adaptive potential and its effects on population persistence to improve decision-making into the future.

Conservation Genetics