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Shawna J Zimmerman

Publications and source records attributed to Shawna J Zimmerman.

17 recordsLinked to original sources

Predicted genetic consequences of alternative population control strategies for North American plains bison in Yellowstone National Park

North American plains bison ( Bison bison bison ) in Yellowstone National Park are descendant from a population low of 23 indigenous individuals from the late 1800s, and 21 individuals introduced from outside herds in the early 1900s to strengthen the possibility of recovery. Within the park, the herd has rebounded and now averages around 5,000 animals. The herd is managed as a closed population within the park and adjacent areas in Montana, USA, which involves annual removals of animals to control numbers. We used genetic simulation to first isolate the effects of population size on retention of genetic diversity, and second to predict the genetic consequences of different population control strategies that vary in the number of bison removed annually, and their relatedness, while considering varying degrees of male dominance and environmental catastrophes. We found through simulation of a stable population that a herd size >2,500 had a high probability (>0.9) of retaining genetic diversity at levels compatible with long-term conservation (>90% of the initial genetic variation over 200 years), but a herd of 3,500 or more had a high likelihood (>0.9) of retaining levels of genetic variation (95%) suggested for maintaining evolutionary potential. When simulating the removals based on plausible management strategies available to the National Park Service, we found that maintaining a herd size of 3,500 or more, limiting removals to less than 40% of the population at a time, keeping a balanced sex ratio, and preferentially removing related individuals would likely retain more than 95% of existing genetic variation. With a herd size of 3,500 animals or more, population catastrophes and male dominance only influenced genetic retention in the most extreme cases, such as a catastrophic population decline of over 95%, a prolonged decline from 90% to 10% over 5 years, or extreme male dominance where 1% of males produced all offspring each year.

Idaho, Montana, Wyoming

Bovine SNP array-based genetic assessment of American plains bison at American Prairie

American plains bison ( Bison bison bison , bison hereafter) experienced an extreme demographic bottleneck in the late 1800s. The species has since rebounded but is primarily managed as small and isolated herds due to habitat and sociopolitical limitations. Thus, reintroducing bison and allowing herds to achieve as much of their natural dynamics as possible is a major conservation goal. Concerns about genetic diversity loss in small, isolated herds and the persistence of cattle-origin variants from historical crossbreeding efforts have made genetic analysis an important part of bison conservation. The limitations of the current conservation genetic tools which are based on traditional markers such as microsatellites and mitochondrial DNA sequences, may be overcome with genome-wide genotyping panels commonly developed for agricultural species. Bison reintroduction in the grasslands at American Prairie began in 2005. Genetic analysis on these herds has yet to be conducted. We used the Illumina 777K Bovine genotyping panel to obtain data from 197 bison and 179 domestic cows to understand the current population genetic state of bison at American Prairie and gain insight on cattle ( Bos taurus ) introgression. Overall, bison at American Prairie currently have relatively high genetic diversity, low inbreeding, and no obvious signs of cattle introgression. A more comprehensive evaluation of introgression, likely including whole-genome sequence data, would clarify this finding. These results can serve as a baseline for future comparison as part of a genetic monitoring framework.

Journal of Heredity

Assessing shifting technology in genetic monitoring of the North American plains bison Federal conservation herds

Human expansion is a major driver of both declining wildlife abundance and the contraction of species’ distributions, increasing the risk of genetic erosion and the need for genetic monitoring. Rapidly advancing technology has expanded the types of genetic data that are available for wildlife conservation. However, inferences from different genetic markers could result in different management decisions and, thus, must be considered carefully. Rebounding from near extinction in the early 1900s, the majority of North American plains bison ( Bison bison bison ) are managed as small and isolated herds. Microsatellite-based analyses have been used to inform management of the US Federal bison conservation herds since the early 2000s. Transitioning from monitoring with tens of multiallelic loci (e.g., microsatellite loci) to thousands of biallelic loci (e.g., single nucleotide polymorphisms [SNPs]) could increase genotyping efficiency and improve the precision of population genetic inference but would require an understanding of the inferential differences between genetic marker types. We compared microsatellite-based measures of genetic diversity, differentiation, and population structure for 20 bison conservation herds (17 Federal, 1 Tribal, 2 Canadian) to inference from SNP-based analyses for the Tribal herd and 15 of the Federal herds. Data from both genetic marker types found that all herds have remarkably high genetic diversity given the severity of the bottleneck from which these populations recovered, and that population structure was consistent with founding histories. Importantly, SNPs had greater power to describe differences in genetic diversity and groups of related herds, but only if analyses are based on 250 or more loci. Overall, we found that microsatellite and SNP data can provide comparable conservation insight, but SNPs must be carefully selected to ensure continuity in genetic monitoring and to achieve the increased precision in genetic diversity and differentiation among herds that we observed in this study.

Conservation Genetics

Cgsim: An R package for simulation of population genetics for conservation and management applications

Wildlife conservation and management increasingly considers genetic information to plan, understand and evaluate implemented population interventions. These actions commonly include conservation translocation and population reductions through removals. Change in genetic variation in response to management actions can be unintuitive due to the influence of multiple interacting drivers (e.g. genetic drift, life history traits, environmental stochasticity). Simulation is an excellent tool to understand the predicted consequences of different proposed or implemented actions. However, the genetic simulators that are robust to a wide variety of life history traits also have a steep learning curve to appropriately parameterize common management actions. To fill this gap, we have developed cgsim, an R package for simulating the genetic consequences of common management interventions for populations of wildlife species. We developed a set of functions to specifically understand the effects of four main aspects of managing small, declining or isolated populations: loss of genetic diversity to drift, augmenting existing populations (e.g. translocation), population reduction through targeted removals and population catastrophes driven by stochastic extrinsic forces. Our single population simulation model is individual-based, and flexible to a range of life history traits. Here we validate cgsim through comparison of simulations to theoretical expectations of genetic diversity loss and illustrate its applied utility by focusing on a recently published empirical example for the Greater Sage-Grouse. Cgsim is available as an R package at: https://doi.org/10.5066/P1BXBEXJ .

Molecular Ecology Resources

The potential influence of genome-wide adaptive divergence on conservation translocation outcome in an isolated greater sage-grouse population

Conservation translocations are an important conservation tool commonly employed to augment declining or reestablish extirpated populations. One goal of augmentation is to increase genetic diversity and reduce the risk of inbreeding depression (i.e., genetic rescue). However, introducing individuals from significantly diverged populations risks disrupting coadapted traits and reducing local fitness (i.e., outbreeding depression). Genetic data are increasingly more accessible for wildlife species and can provide unique insight regarding the presence and retention of introduced genetic variation from augmentation as an indicator of effectiveness and adaptive similarity as an indicator of source and recipient population suitability. We used 2 genetic data sets to evaluate augmentation of isolated populations of greater sage-grouse ( Centrocercus urophasianus ) in the northwestern region of the species range (Washington, USA) and to retrospectively evaluate adaptive divergence among source and recipient populations. We developed 2 statistical models for microsatellite data to evaluate augmentation outcomes. We used one model to predict genetic diversity after augmentation and compared these predictions with observations of genetic change. We used the second model to quantify the amount of observed reproduction attributed to transplants (proof of population integration). We also characterized genome-wide adaptive divergence among source and recipient populations. Observed genetic diversity ( H O = 0.65) was higher in the recipient population than predicted had no augmentation occurred ( H O = 0.58) but less than what was predicted by our model ( H O = 0.75). The amount of shared genetic variation between the 2 geographically isolated resident populations increased, which is evidence of periodic gene flow previously assumed to be rare. Among candidate adaptive genes associated with elevated fixation index ( F ST ) (143 genes) or local environmental variables (97 and 157 genes for each genotype–environment association method, respectively), we found clusters of genes with related functions that may influence the ability of transplants to use local resources and navigate unfamiliar environments and their reproductive potential, all possible reasons for low genetic retention from augmentation.

Conservation Biology

Genetic Connectivity in the Arizona toad (Anaxyrus microscaphus): implications for conservation of a stream dwelling amphibian in the arid Southwestern U.S.

The Arizona Toad ( Anaxyrus microscaphus ) is restricted to riverine corridors and adjacent uplands in the arid southwestern United States. As with numerous amphibians worldwide, populations are declining and face various known or suspected threats, from disease to habitat modification resulting from climate change. The Arizona Toad has been petitioned to be listed under the U.S. Endangered Species Act and was considered “warranted but precluded” citing the need for additional information – particularly regarding natural history (e.g., connectivity and dispersal ability). The objectives of this study were to characterize population structure and genetic diversity across the species’ range. We used reduced-representation genomic sequencing to genotype 3,601 single nucleotide polymorphisms in 99 Arizona Toads from ten drainages across its range. Multiple analytical methods revealed two distinct genetic groups bisected by the Colorado River; one in the northwestern portion of the range in southwestern Utah and eastern Nevada and the other in the southeastern portion of the range in central and eastern Arizona and New Mexico. We also found subtle substructure within both groups, particularly in central Arizona where toads at lower elevations were less connected than those at higher elevations. The northern and southern parts of the Arizona Toad range are not well connected genetically and could be managed as separate units. Further, these data could be used to identify source populations for assisted migration or translocations to support small or potentially declining populations.

Arizona, Nevada, New Mexico

A metapopulation strategy to support long term conservation of genetic diversity in Department of the Interior bison

Once numbering in the tens of millions, plains bison ( Bison bison bison ) were nearly driven to extinction with only a few hundred individuals remaining by the late 19th century. Plains bison have since recovered to approximately 20,000 animals managed in conservation herds throughout North America, yet substantial challenges to their recovery remain. The Department of the Interior (DOI) is working with diverse partners to steward approximately 11,000 bison in 18 conservation herds across 12 states. Most herds exist in areas without native predators, and removals are required to keep herd sizes at or below carrying capacity. The loss of genetic diversity within bison, and the fact that most DOI herds are relatively small and isolated from each other with no opportunity for natural gene flow, raises concerns about maintaining genetic diversity over the long term. Connecting populations through gene flow (i.e., creating a metapopulation) can minimize loss of genetic diversity, both within and across populations. Management of DOI bison conservation herds has historically varied across bureaus and conservation units. Adopting a national perspective on bison conservation was identified as a priority in the 2008 Department of the Interior Bison Conservation Initiative (BCI). The concept of metapopulation management as a potential tool to maximize the conservation of genetic diversity among DOI herds was first described in this 2008 Initiative and was specifically encouraged in the 2010 DOI Bison Conservation Genetics Workshop report (Dratch and Gogan 2010). In the 2020 BCI, the DOI re-affirmed its commitment to conserving bison as native, North American wildlife. This document establishes a framework for a nationally coordinated strategy for bison managed by the DOI to support the genetic conservation goals outlined in the 2020 BCI. This is a decisionmaking framework that guides managers through the process of determining when and how to consider translocations. Decisions and actions within the framework are informed by analysis and interpretation of data housed in an integrated, relational database that will be initially populated with the most current data and updated annually thereafter. It provides science-based guidance on how to conserve DOI bison genetic diversity through strategic translocations, while also considering cattle introgression and bison health. We illustrate how this Strategy can be used to guide the establishment of new conservation herds and discuss what it means to be a DOI partner. Finally, this is intended to be used as a living document that will evolve as needs and technologies change.

Science Report

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

A genetic warning system for a hierarchically structured wildlife monitoring framework

Genetic variation is a well-known indicator of population fitness yet is not typically included in monitoring programs for sensitive species. Additionally, most programs monitor populations at one scale, which can lead to potential mismatches with ecological processes critical to species' conservation. Recently developed methods generating hierarchically nested population units (i.e., clusters of varying scales) for greater sage-grouse ( Centrocercus urophasianus ) have identified population trend declines across spatiotemporal scales to help managers target areas for conservation. The same clusters used as a proxy for spatial scale can alert managers to local units (i.e., neighborhood-scale) with low genetic diversity, further facilitating identification of management targets. We developed a genetic warning system utilizing previously developed hierarchical population units to identify management-relevant areas with low genetic diversity within the greater sage-grouse range. Within this warning system we characterized conservation concern thresholds based on values of genetic diversity and developed a statistical model for microsatellite data to robustly estimate these values for hierarchically nested populations. We found that 41 of 224 neighborhood-scale clusters had low genetic diversity, 23 of which were coupled with documented local population trend decline. We also found evidence of cross-scale low genetic diversity in the small and isolated Washington population, unlikely to be reversed through typical local management actions alone. The combination of low genetic diversity and a declining population suggests relatively high conservation concern. Our findings could further facilitate conservation action prioritization in combination with population trend assessments and (or) local information, and act as a base-line of genetic diversity for future comparison. Importantly, the approach we used is broadly applicable across taxa.

Ecological Applications

Simulation of genetic change under four removal strategies for a wild horse population

Small and/or artificially reduced populations can suffer genetic erosion with long-term consequences to population fitness and persistence. However, managers must periodically remove free-roaming horses from the landscape to reduce the risk of habitat degradation. We developed an individual-based population simulation model to evaluate the expected change in genetic diversity after 100 years under each of four removal strategies for the wild horse population in the Pryor Mountain management area with removals occurring every 5 years, and assuming that no additional horses are introduced to the herd. We found that long generations and high survival rates of this wild horse population guard against rapid loss of genetic diversity for all scenarios in general. However, scenarios that included a removal strategy prioritizing individuals for removal based on relatedness initially increased mean genetic diversity that was subsequently maintained at a higher level than strategies that randomly selected individuals for removal.

Report

Scale-dependent influence of the sagebrush community on genetic connectivity of the sagebrush obligate Gunnison sage-grouse

Habitat fragmentation and degradation impacts an organism's ability to navigate the landscape, ultimately resulting in decreased gene flow and increased extinction risk. Understanding how landscape composition impacts gene flow (i.e., connectivity) and interacts with scale is essential to conservation decision-making. We used a landscape genetics approach implementing a recently developed statistical model based on the generalized Wishart probability distribution to identify the primary landscape features affecting gene flow and estimate the degree to which each component influences connectivity for Gunnison sage-grouse ( Centrocercus minimus ). We were interested in two spatial scales: among distinct populations rangewide and among leks (i.e., breeding grounds) within the largest population, Gunnison Basin. Populations and leks are nested within a landscape fragmented by rough terrain and anthropogenic features, although requisite sagebrush habitat is more contiguous within populations. Our best fit models for each scale confirm the importance of sagebrush habitat in connectivity, although the important sagebrush characteristics differ. For Gunnison Basin, taller shrubs and higher quality nesting habitat were the primary drivers of connectivity, while more sagebrush cover and less conifer cover facilitated connectivity rangewide. Our findings support previous assumptions that Gunnison sage-grouse range contraction is largely the result of habitat loss and degradation. Importantly, we report direct estimates of resistance for landscape components that can be used to create resistance surfaces for prioritization of specific locations for conservation or management (i.e., habitat preservation, restoration, or development) or as we demonstrated, can be combined with simulation techniques to predict impacts to connectivity from potential management actions.

Colorado, Utah

Environmental gradients of selection for an alpine-obligate bird, the white-tailed ptarmigan (Lagopus leucura)

The warming climate will expose alpine species adapted to a highly seasonal, harsh environment to novel environmental conditions. A species can shift their distribution, acclimate, or adapt in response to a new climate. Alpine species have little suitable habitat to shift their distribution, and the limits of acclimation will likely be tested by climate change in the long-term. Adaptive genetic variation may provide the raw material for species to adapt to this changing environment. Here, we use a genomic approach to describe adaptive divergence in an alpine-obligate species, the white-tailed ptarmigan ( Lagopus leucura ), a species distributed from Alaska to New Mexico, across an environmentally variable geographic range. Previous work has identified genetic structure and morphological, behavioral, and physiological differences across the species’ range; however, those studies were unable to determine the degree to which adaptive divergence is correlated with local variation in environmental conditions. We used a genome-wide dataset generated from 95 white-tailed ptarmigan distributed throughout the species’ range and genotype–environment association analyses to identify the genetic signature and environmental drivers of local adaptation. We detected associations between multiple environmental gradients and candidate adaptive loci, suggesting ptarmigan populations may be locally adapted to the plant community composition, elevation, local climate, and to the seasonality of the environment. Overall, our results suggest there may be groups within the species’ range with genetic variation that could be essential for adapting to a changing climate and helpful in guiding conservation action.

Alaska, Washington, Montana, Colorado, New Mexico,

An empirical comparison of population genetic analyses using microsatellite and SNP data for a species of conservation concern

Background Use of genomic tools to characterize wildlife populations has increased in recent years. In the past, genetic characterization has been accomplished with more traditional genetic tools (e.g., microsatellites). The explosion of genomic methods and the subsequent creation of large SNP datasets has led to the promise of increased precision in population genetic parameter estimates and identification of demographically and evolutionarily independent groups, as well as questions about the future usefulness of the more traditional genetic tools. At present, few empirical comparisons of population genetic parameters and clustering analyses performed with microsatellites and SNPs have been conducted. Results Here we used microsatellite and SNP data generated from Gunnison sage-grouse ( Centrocercus minimus ) samples to evaluate concordance of the results obtained from each dataset for common metrics of genetic diversity ( H O , H E , F IS , A R ) and differentiation ( F ST , G ST , D Jost ). Additionally, we evaluated clustering of individuals using putatively neutral (SNPs and microsatellites), putatively adaptive, and a combined dataset of putatively neutral and adaptive loci. We took particular interest in the conservation implications of any differences. Generally, we found high concordance between microsatellites and SNPs for H E , F IS , A R , and all differentiation estimates. Although there was strong correlation between metrics from SNPs and microsatellites, the magnitude of the diversity and differentiation metrics were quite different in some cases. Clustering analyses also showed similar patterns, though SNP data was able to cluster individuals into more distinct groups. Importantly, clustering analyses with SNP data suggest strong demographic independence among the six distinct populations of Gunnison sage-grouse with some indication of evolutionary independence in two or three populations; a finding that was not revealed by microsatellite data. Conclusion We demonstrate that SNPs have three main advantages over microsatellites: more precise estimates of population-level diversity, higher power to identify groups in clustering methods, and the ability to consider local adaptation. This study adds to a growing body of work comparing the use of SNPs and microsatellites to evaluate genetic diversity and differentiation for a species of conservation concern with relatively high population structure and using the most common method of obtaining SNP genotypes for non-model organisms.

Arizona, Colorado, New Mexico, Utah

The transformative impact of genomics on sage-grouse conservation and management

For over two decades, genetic studies have been used to assist in the conservation and management of both Greater Sage-grouse ( Centrocercus urophasianus ) and Gunnison Sage-grouse ( C. minimus ), addressing a wide variety of topics including taxonomy, parentage, population connectivity, and demography. The field of conservation genetics has been transformed by dramatic improvements in sequencing technology, facilitating genomic studies in many wildlife species. The quality and amount of data generated by genomic methods vastly exceed that of traditional genetic studies, allowing for increased precision in estimating genetic parameters of interest. Perhaps more importantly, genomic methods can provide insight into non-neutral evolution such as adaptive divergence. Here we recount the shift from genetic to genomic methods using two wildlife species of substantial conservation interest, focusing on the improved capabilities and advantages of genomic methods. For instance, reassessment of divergence in sage-grouse using genomic methods confirmed strong differentiation between the two species and revealed that a small population in the state of Washington was more genetically distinct than previously recognized. Further, new genomic resources and approaches have been used to identify a family of genes linked to local dietary adaptation suggesting that sage-grouse may possess digestive and metabolic adaptations that mitigate the effects of consuming plant secondary metabolites like those found in sagebrush. Genetic variation among populations in these gene regions is thought to be involved with local dietary adaptations, and therefore maintaining the tie between sage-grouse and the chemistry of local sagebrush may be an important management consideration. We posit that the integration of newly developed genomic resources combined with the vast wealth of ecological and behavioral data for sage-grouse has the potential to shed light on mechanistic relationships that ultimately are vital to the conservation and management of these species.

Book chapter

Signatures of adaptive divergence among populations of an avian species of conservation

Understanding the genetic underpinning of adaptive divergence among populations is a key goal of evolutionary biology and conservation. Gunnison sage‐grouse ( Centrocercus minimus ) is a sagebrush obligate species with a constricted range consisting of seven discrete populations, each with distinctly different habitat and climatic conditions. Though geographically close, populations have low levels of natural gene flow resulting in relatively high levels of differentiation. Here, we use 15,033 SNP loci in genomic outlier analyses, genotype–environment association analyses, and gene ontology enrichment tests to examine patterns of putatively adaptive genetic differentiation in an avian species of conservation concern. We found 411 loci within 5 kbp of 289 putative genes associated with biological functions or pathways that were overrepresented in the assemblage of outlier SNPs. The identified gene set was enriched for cytochrome P450 gene family members (CYP4V2, CYP2R1, CYP2C23B, CYP4B1) and could impact metabolism of plant secondary metabolites, a critical challenge for sagebrush obligates. Additionally, the gene set was also enriched with members potentially involved in antiviral response (DEAD box helicase gene family and SETX). Our results provide a first look at local adaption for isolated populations of a single species and suggest adaptive divergence in multiple metabolic and biochemical pathways may be occurring. This information can be useful in managing this species of conservation concern, for example, to identify unique populations to conserve, avoid translocation or release of individuals that may swamp locally adapted genetic diversity, or guide habitat restoration efforts.

Arizona, Colorado, New Mexico, Utah

Evaluation of genetic change from translocation among Gunnison Sage-Grouse (Centrocercus minimus) populations

Maintenance of genetic diversity is important for conserving species, especially those with fragmented habitats or ranges. In the absence of natural dispersal, translocation can be used to achieve this goal, although the success of translocation can be difficult to measure. Here we evaluate genetic change following translocation in Gunnison Sage-Grouse ( Centrocercus minimus ), a species reduced to 7 discrete populations with low levels of gene flow and high levels of genetic differentiation. Between 2000 and 2014, 306 birds from the largest and most genetically diverse population (Gunnison Basin) were translocated to 5 much smaller satellite populations to augment local population size and increase genetic diversity. Although the magnitude of the effect varied by population, we found evidence of increased genetic variation, decreased genetic differentiation from Gunnison Basin, and reproduction between translocated individuals and resident birds. These results suggest that translocations are impacting satellite populations, with current data providing a new baseline for genetic diversity among populations of this imperiled species.

Colorado, Utah

Development of 13 microsatellites for Gunnison Sage-grouse ( Centrocercus minimus ) using next-generation shotgun sequencing and their utility in Greater Sage-grouse ( Centrocercus urophasianus )

Gunnison Sage-grouse are an obligate sagebrush species that has experienced significant population declines and has been proposed for listing under the U.S. Endangered Species Act. In order to examine levels of connectivity among Gunnison Sage-grouse leks, we identified 13 novel microsatellite loci though next-generation shotgun sequencing, and tested them on the closely related Greater Sage-grouse. The number of alleles per locus ranged from 2 to 12. No loci were found to be linked, although 2 loci revealed significant departures from Hardy–Weinberg equilibrium or evidence of null alleles. While these microsatellites were designed for Gunnison Sage-grouse, they also work well for Greater Sage-grouse and could be used for numerous genetic questions including landscape and population genetics.

Conservation Genetics Resources