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USGS2011

Guidelines for collecting and maintaining archives for genetic monitoring

Rapid advances in molecular genetic techniques and the statistical analysis of genetic data have revolutionized the way that populations of animals, plants and microorganisms can be monitored. Genetic monitoring is the practice of using molecular genetic markers to track changes in the abundance, diversity or distribution of populations, species or ecosystems over time, and to follow adaptive and non-adaptive genetic responses to changing external conditions. In recent years, genetic monitoring has become a valuable tool in conservation management of biological diversity and ecological analysis, helping to illuminate and define cryptic and poorly understood species and populations. Many of the detected biodiversity declines, changes in distribution and hybridization events have helped to drive changes in policy and management. Because a time series of samples is necessary to detect trends of change in genetic diversity and species composition, archiving is a critical component of genetic monitoring. Here we discuss the collection, development, maintenance, and use of archives for genetic monitoring. This includes an overview of the genetic markers that facilitate effective monitoring, describes how tissue and DNA can be stored, and provides guidelines for proper practice.

Conservation Genetics Resources↗

USGS2010

A population genetic analysis of the midget faded rattlesnake in Wyoming

Little is known about the population biology of midget faded rattlesnakes, a sensitive subspecies of the Western Rattlesnake, despite conservation efforts to protect them. We conducted a molecular genetic study of midget faded rattlesnakes in southwestern Wyoming to investigate population genetic structure in this area, particularly with reference to Flaming Gorge Reservoir and its associated human activities, and to document levels of genetic diversity. We genotyped 229 snakes from 11 sampling sites using 9 microsatellite loci. We found significant levels of genetic structure among sites that were better explained by geographic region and isolation by distance than by position relative to waterways. Sites on either side of the reservoir at its widest point were not significantly different. Six of the sites showed signatures of a population bottleneck using an alpha value of 0.05. Three of these bottlenecked sites (the three most northern) were the most genetically distinct and occur in areas of greatest impact from human activity.

Wyoming↗

USGS2017

Microsatellite marker development from next-generation sequencing in the New England cottontail (Sylvilagus transitionalis) and cross-amplification in the eastern cottontail (S. floridanus)

Objective The New England cottontail ( Sylvilagus transitionalis ) is a species of high conservation priority in the Northeastern United States, and was a candidate for federal listing under the Endangered Species Act until a recent decision determined that conservation actions were sufficient to preclude listing. The aim of this study was to develop a suite of microsatellite loci to guide future research efforts such as the analysis of population genetic structure, genetic variation, dispersal, and genetic mark-recapture population estimation. Results Thirty-five microsatellite markers containing tri- and tetranucleotide sequences were developed from shotgun genomic sequencing of tissue from S. transitionalis , S. obscurus , and S. floridanus . These loci were screened in n = 33 wild S. transitionalis sampled from a population in eastern Massachusetts, USA. Thirty-two of the 35 loci were polymorphic with 2–6 alleles, and observed heterozygosities of 0.06–0.82. All loci conformed to Hardy–Weinberg Equilibrium proportions and there was no evidence of linkage disequilibrium or null alleles. Primers for 33 of the 35 loci amplified DNA extracted from n = 6 eastern cottontail ( S. floridanus ) samples, of which nine revealed putative species-diagnostic alleles. These loci will provide a useful tool for conservation genetics investigations of S. transitionalis and a potential diagnostic species assay for differentiating sympatric eastern and New England cottontails.

Massachusetts↗

USGS2001

Evaluation of the major histocompatibility complex (Mhc) in cranes: applications to conservation efforts

Although there have been heated discussions concerning the relative importance of using Mhc diversity as a basis for selecting breeders in conservation projects, most parties agree that the genetic variability residual in an endangered species should be maintained through genetic management, if at all possible. Substantial evidence exists (particularly in birds) documenting the influences of specific Mhc haplotypes on disease outcome and also that those individuals which are heterozygous for Mhc alleles appear to have an advantage for survival over those that are homozygous. Thus, conservation of genetic variability of the Mhc is likely important for the preservation of fitness, especially in small breeding populations. More than half of the world's crane species are listed as endangered. Members of all 15 known species are represented among breeding animals for captive propagation at the International Crane Foundation (Wisconsin) and the USGS Patuxent Wildlife Research Center (Maryland). Collaborative multi-organization efforts and the availability of extensive pedigree records have allowed the study of Mhc variability in several species of cranes. We have found, for example, that Mhc diversity in the captive Florida sandhill crane (Grus canadensis pratensis) population appears high, whereas in the captive whooping crane (Grus americana), which has undergone a severe 'genetic bottleneck,? both the number of alleles and the levels of heterozygosity appear to be substantially reduced.

Book chapter↗

USGS2001

Geographic variation and genetic structure in Spotted Owls

We examined genetic variation, population structure, and definition of conservation units in Spotted Owls ( Strix occidentalis ). Spotted Owls are mostly non-migratory, long-lived, socially monogamous birds that have decreased population viability due to their occupation of highly-fragmented late successional forests in western North America. To investigate potential effects of habitat fragmentation on population structure, we used random amplified polymorphic DNA (RAPD) to examine genetic variation hierarchically among local breeding areas , subregional groups , regional groups , and subspecies via sampling of 21 breeding areas (276individuals) among the three subspecies of Spotted Owls. Data from 11 variable bands suggest a significant relationship between geographic distance among local breeding groups and genetic distance (Mantel r = 0.53, P < 0.02) although multi-dimensional scaling of three significant axes did not identify significant grouping at any hierarchical level. Similarly, neighbor-joining clustering of Manhattan distances indicated geographic structure at all levels and identified Mexican Spotted Owls as a distinct clade. RAPD analyses did not clearly differentiate Northern Spotted Owls from California Spotted Owls. Among Northern Spotted Owls, estimates of population differentiation (F ST ) ranged from 0.27 among breeding areas to 0.11 among regions. Concordantly, within-group agreement values estimated via multi-response permutation procedures of Jaccard's distances ranged from0.22 among local sites to 0.11 among regions. Pairwise comparisons of F ST and geographic distance within regions suggested only the Klamath region was in equilibrium with respect to gene flow and genetic drift. Merging nuclear data with recent mitochondrial data provides support for designation of an Evolutionary Significant Unit for Mexican Spotted Owls and two overlapping Management Units for Northern and California Spotted Owls.

Conservation Genetics↗

USGS2016

Climate variables explain neutral and adaptive variation within salmonid metapopulations: The importance of replication in landscape genetics

Understanding how environmental variation influences population genetic structure is important for conservation management because it can reveal how human stressors influence population connectivity, genetic diversity and persistence. We used riverscape genetics modelling to assess whether climatic and habitat variables were related to neutral and adaptive patterns of genetic differentiation (population-specific and pairwise F ST ) within five metapopulations (79 populations, 4583 individuals) of steelhead trout ( Oncorhynchus mykiss ) in the Columbia River Basin, USA. Using 151 putatively neutral and 29 candidate adaptive SNP loci, we found that climate-related variables (winter precipitation, summer maximum temperature, winter highest 5% flow events and summer mean flow) best explained neutral and adaptive patterns of genetic differentiation within metapopulations, suggesting that climatic variation likely influences both demography (neutral variation) and local adaptation (adaptive variation). However, we did not observe consistent relationships between climate variables and F ST across all metapopulations, underscoring the need for replication when extrapolating results from one scale to another (e.g. basin-wide to the metapopulation scale). Sensitivity analysis (leave-one-population-out) revealed consistent relationships between climate variables and F ST within three metapopulations; however, these patterns were not consistent in two metapopulations likely due to small sample sizes ( N = 10). These results provide correlative evidence that climatic variation has shaped the genetic structure of steelhead populations and highlight the need for replication and sensitivity analyses in land and riverscape genetics.

Columbia River Basin↗

USGS2004

Fort Collins Science Center: Species and Habitats of Federal Interest

Ecosystem changes directly affect a wide variety of plant and animal species, floral and faunal communities, and groups of species such as amphibians and grassland birds. Appropriate management of public lands plays a crucial role in the conservation and recovery of endangered species and can be a key element in preventing a species from being listed under the Endangered Species Act. The Species and Habitats of Federal Interest Branch of the Fort Collins Science Center (FORT) conducts research on the ecology, habitat requirements, distribution and abundance, population dynamics, and genetics and systematics of many species facing threatened or endangered status or of special concern to resource management agencies. FORT scientists develop reintroduction and restoration techniques, technologies for monitoring populations, and novel methods to analyze data on population trends and habitat requirements. FORT expertise encompasses both traditional and specialized natural resource disciplines within wildlife biology, including population dynamics, animal behavior, plant and community ecology, inventory and monitoring, statistics and computer applications, conservation genetics, stable isotope analysis, and curatorial expertise.

Fact Sheet↗

USGS2023

A pragmatic approach for integrating molecular tools into biodiversity conservation

Molecular tools are increasingly applied for assessing and monitoring biodiversity and informing conservation action. While recent developments in genetic and genomic methods provide greater sensitivity in analysis and the capacity to address new questions, they are not equally available to all practitioners: There is considerable bias across institutions and countries in access to technologies, funding, and training. Consequently, in many cases, more accessible traditional genetic data (e.g., microsatellites) are still utilized for making conservation decisions. Conservation approaches need to be pragmatic by tackling clearly defined management questions and using the most appropriate methods available, while maximizing the use of limited resources. Here we present some key questions to consider when applying the molecular toolbox for accessible and actionable conservation management. Finally, we highlight a number of important steps to be addressed in a collaborative way, which can facilitate the broad integration of molecular data into conservation.

Conservation Science and Practice↗

USGS2015

Evidence of low genetic variation and rare alleles in a bottlenecked endangered island endemic, the Lasan Teal (Anas laysanensis)

Genetic diversity is assumed to reflect the evolutionary potential and adaptability of populations, and thus quantifying the genetic diversity of endangered species is useful for recovery programs. In particular, if conservation strategies include reintroductions, periodic genetic assessments are useful to evaluate whether management efforts have resulted in the maximization or loss of genetic variation within populations over generations. In this study, we collected blood, feather, and tissue samples during 1999–2009 and quantified genetic diversity for a critically endangered waterfowl species endemic to the Hawaiian archipelago, the Laysan teal or duck (Anas laysanensis; n = 239 individual birds sampled). The last extant population of this species at Laysan Island was sourced in 2004–2005 for a ‘wild to wild’ translocation of 42 individuals for an experimental reintroduction to Midway Atoll. To inform future management strategies, we compared genetic diversity sampled from the source population (n = 133 Laysan birds) including 23 of Midway’s founders and offspring of the translocated population 2–5 years post release (n = 96 Midway birds). We attempted to identify polymorphic markers by screening nuclear microsatellite (N = 83) and intronic loci (N = 19), as well as the mitochondrial control region (mtDNA) for a subset of samples. Among 83 microsatellite loci screened, six were variable. We found low nuclear variation consistent with the species’ historical population bottlenecks and sequence variation was observed at a single intron locus. We detected no variation within the mtDNA. We found limited but similar estimates of allelic richness (2.58 alleles per locus) and heterozygosity within islands. Two rare alleles found in the Laysan Island source population were not present in the Midway translocated group, and a rare allele was discovered in an individual on Midway in 2008. We found similar genetic diversity and low, but statistically significant, levels of differentiation (0.6%) between island populations suggesting that genetic drift (as a result of translocation-induced population bottlenecking) has had a limited effect within five years post-release. Our results have utility for informing translocation and genetic management decisions.

Hawaii↗

USGS2012

Low genetic diversity and minimal population substructure in the endangered Florida manatee: implications for conservation

Species of management concern that have been affected by human activities typically are characterized by low genetic diversity, which can adversely affect their ability to adapt to environmental changes. We used 18 microsatellite markers to genotype 362 Florida manatees (Trichechus manatus latirostris), and investigated genetic diversity, population structure, and estimated genetically effective population size (Ne). The observed and expected heterozygosity and average number of alleles were 0.455 ± 0.04, 0.479 ± 0.04, and 4.77 ± 0.51, respectively. All measures of Florida manatee genetic diversity were less than averages reported for placental mammals, including fragmented or nonideal populations. Overall estimates of differentiation were low, though significantly greater than zero, and analysis of molecular variance revealed that over 95% of the total variance was among individuals within predefined management units or among individuals along the coastal subpopulations, with only minor portions of variance explained by between group variance. Although genetic issues, as inferred by neutral genetic markers, appear not to be critical at present, the Florida manatee continues to face demographic challenges due to anthropogenic activities and stochastic factors such as red tides, oil spills, and disease outbreaks; these can further reduce genetic diversity of the manatee population.

Journal of Mammalogy↗

USGS2023

A 37 K SNP array for the management and conservation of Golden Eagles (Aquila chrysaetos)

We describe the development of a custom 37 K Affymetrix Axiom myDesign single nucleotide polymorphism (SNP) array for a culturally and ecologically important apex predator, the golden eagle ( Aquila chrysaetos ). Using this SNP array, we performed population genomic analysis on 154 individuals of known natal localities and detected three genetic clusters that we designated as Taiga/High Arctic, Great Basin, and Rocky Mountains/Great Plains. Each of these clusters appears to display clinal variation within these geographic regions. After determining genetic structure, we performed an assignment test of 32 individuals, five of which were siblings of individuals used in the assessment of genetic structure, three had associated telemetry data, and the remaining individuals were of unknown natal locations. Using this array, four siblings were correctly assigned to the same geographic region as their sibling and the genetic assignment of the radio telemetered birds agreed with the expected movement patterns displayed by these individuals. For the remaining individuals, we were able to assign all but five individuals to one of the three genetic clusters. Our genetic assignments illustrates the utility of this SNP array to accurately assign most individuals to predesignated geographical regions. While further compiling genetic and other data types, we can increase the power of this tool for identifying those breeding populations that may need assistance due to anthropogenic stressors that negatively impact their population viability. The use of this genetic resource will help substantiate decisions by multiple conservation groups that seek to preserve the natural population structure of the golden eagle.

Conservation Genetics↗

USGS2021

Establishment of a microsatellite genetic baseline for North American Atlantic sturgeon (Acipenser o. oxyrhinchus) and range-wide analysis of population genetics

Atlantic sturgeon ( Acipenser oxyrinchus oxyrinchus ) is a long-lived, anadromous species that is broadly distributed along the Atlantic coast of North America. Historic overharvest and habitat degradation resulted in significant declines to Atlantic sturgeon populations and, following decades of limited recovery, the species was listed under the Endangered Species Act of the United States in 2012. Given continued threats to recovery and limited information about population demography, there is a need for new tools to assist in Atlantic sturgeon conservation. Here, we present a range-wide microsatellite genetic baseline for North American Atlantic sturgeon that is comprised of 2510 individuals from 18 genetically distinct groups collected in 13 rivers and one estuary. Analysis of this baseline suggested that populations from the northern range of Atlantic sturgeon were more highly differentiated than those from the southern extent, where patterns of differentiation were complicated by rivers with genetically distinct spring and fall spawning runs and less geographic distance separating populations. Despite significant demographic bottleneck events, all populations showed at least moderate levels of genetic diversity across a suite of metrics. Additionally, individual-based assignment tests had over 80% accuracy for assigning individuals to their river of origin, highlighting the utility of this baseline for characterizing the composition of mixed-stock aggregations and understanding stock-specific vulnerability and recovery. The expanded spatial coverage of this baseline dataset enabled novel inferences about patterns of genetic differentiation and spawning phenology in Atlantic sturgeon which can be used to support conservation and management efforts.

Atlantic Coast↗

USGS2015

Targeting climate diversity in conservation planning to build resilience to climate change

Climate change is raising challenging concerns for systematic conservation planning. Are methods based on the current spatial patterns of biodiversity effective given long-term climate change? Some conservation scientists argue that planning should focus on protecting the abiotic diversity in the landscape, which drives patterns of biological diversity, rather than focusing on the distribution of focal species, which shift in response to climate change. Climate is one important abiotic driver of biodiversity patterns, as different climates host different biological communities and genetic pools. We propose conservation networks that capture the full range of climatic diversity in a region will improve the resilience of biotic communities to climate change compared to networks that do not. In this study we used historical and future hydro-climate projections from the high resolution Basin Characterization Model to explore the utility of directly targeting climatic diversity in planning. Using the spatial planning tool, Marxan, we designed conservation networks to capture the diversity of climate types, at the regional and sub-regional scale, and compared them to networks we designed to capture the diversity of vegetation types. By focusing on the Conservation Lands Network (CLN) of the San Francisco Bay Area as a real-world case study, we compared the potential resilience of networks by examining two factors: the range of climate space captured, and climatic stability to 18 future climates, reflecting different emission scenarios and global climate models. We found that the climate-based network planned at the sub-regional scale captured a greater range of climate space and showed higher climatic stability than the vegetation and regional based-networks. At the same time, differences among network scenarios are small relative to the variance in climate stability across global climate models. Across different projected futures, topographically heterogeneous areas consistently show greater climate stability than homogenous areas. The analysis suggests that utilizing high-resolution climate and hydrological data in conservation planning improves the likely resilience of biodiversity to climate change. We used these analyses to suggest new conservation priorities for the San Francisco Bay Area.

Ecosphere↗

USGS2020

Refining genetic boundaries for Agassiz’s desert tortoise (Gopherus agassizii) in the western Sonoran Desert: The influence of the Coachella Valley on gene flow among populations in southern California

Understanding the influence of geographic features on the evolutionary history and population structure of a species can assist wildlife managers in delimiting genetic units (GUs) for conservation and management. Landscape features including mountains, low elevation depressions, and even roads can influence connectivity and gene flow among Agassiz’s desert tortoise (Gopherus agassizii) populations. Substantial changes in the landscape of the American Southwest occurred during the last six million years (including the formation of the Gulf of California and the lower Colorado River), which shaped the distribution and genetic structuring of tortoise populations. The area northwest of the Gulf of California is occupied by the Salton Trough, including the Coachella Valley at its northern end. Much of this area is below sea level and unsuitable as tortoise habitat, thus forming a potential barrier for gene flow. We assessed genetic relationships among three tortoise populations separated by the Coachella Valley. Two adjacent populations were on the east side of the valley in the foothills of the Cottonwood and Orocopia mountains separated by Interstate 10. The third population, Mesa, was located about 87 km away in the foothills of the San Bernardino Mountains at the far northwestern tip of the valley. The Cottonwood and Orocopia localities showed genetic affiliation with the adjacent Colorado Desert GU immediately to the east, and the Mesa population exhibited affiliation with both the Southern Mojave and Colorado Desert GUs, despite having a greater geographic distance (0.5x–1.5x greater) to the Colorado Desert GU. The genetic affiliation with the Colorado Desert GU suggests that the boundary for that GU needs to be substantially extended to the west to include the desert tortoise populations around the Coachella Valley. Their inclusion in the Colorado Desert GU may benefit these often overlooked populations when recovery actions are considered.

California↗

USGS2018

Interisland genetic structure of two endangered Hawaiian waterbirds: The Hawaiian Coot and Hawaiian Gallinule

Most of Hawaii's endemic avifauna are species of conservation concern. Some of Hawaii's endangered waterbirds, however, have increased in number as a result of intensive management of wetlands. To inform these conservation efforts, we examined interisland genetic structure and gene flow within 2 Hawaiian endemic waterbirds, the Hawaiian Coot ( Fulica alai ) and the Hawaiian subspecies of the Common Gallinule ( Gallinula galeata sandvicensis ), using microsatellite and mitochondrial loci. Hawaiian Coots and Hawaiian Gallinules occupy coastal wetlands and exhibit similar life history characteristics and generation times, although they may differ in dispersal propensity. Mark–resight data for Hawaiian Coot indicate interisland movements, whereas Hawaiian Gallinules are sedentary. Genetic diversity is partitioned across the landscape differently for Hawaiian Coots and Hawaiian Gallinules; patterns of variation are likely influenced by behavioral and ecological mechanisms. Hawaiian Coots exhibit low levels of structure at microsatellite loci ( F ST = 0.029) and high levels of gene flow among islands. Conversely, Hawaiian Gallinules are highly structured across marker types (microsatellite F ST = 0.205, mtDNA control region F ST = 0.370, mtDNA ND2 F ST = 0.087), with restricted recent gene flow. Patterns of gene flow have changed after the population declines in the early to mid-1900s. Gene flow estimates indicate historical dispersal from Kauai to Oahu in both species, while recent estimates show individual Hawaiian Coots dispersing from Oahu and restricted gene flow between islands for the Hawaiian Gallinule. Changes in gene flow through time suggest that patterns of dispersal may be an artifact of the availability of habitat, which may be indirectly associated with the synergistic influences of population density and wetland quality. Despite recent population size increases for both species, continued threats to Hawaiian waterbirds (i.e. nonnative mammalian predators and invasive plants, avian disease, altered hydrology, and saltwater inundation of freshwater wetlands) will likely require continued active management to maintain viable populations.

Hawaii↗

USGS2025

A survey of mammal and fish genetic diversity across the global protected area network

Global conservation targets aim to expand protected areas and maintain species’ genetic diversity. Whether protected areas capture genetic diversity is unclear. We examined this question using a global sample of nuclear population-level microsatellite data comprising genotypes from 2513 sites, 134,183 individuals, and 176 mammal and marine fish species. The genetic diversity and differentiation of samples inside and outside protected areas were similar, with some evidence for higher diversity in protected areas for small-bodied mammals. Mammal populations, particularly large species, tended to be more genetically diverse when near multiple protected areas, regardless of whether samples were collected in or outside protected areas. Older marine protected areas tended to capture more genetically diverse fish populations. However, limited data availability in many regions hinders the systematic incorporation of genetic diversity into protected area design. Focusing on minimizing population decline and maintaining connectivity between protected areas remain essential proxies for maintaining genetic diversity.

Conservation Letters↗

USGS2017

Climate change refugia and habitat connectivity promote species persistence

Background Climate change refugia, areas buffered from climate change relative to their surroundings, are of increasing interest as natural resource managers seek to prioritize climate adaptation actions. However, evidence that refugia buffer the effects of anthropogenic climate change is largely missing. Methods Focusing on the climate-sensitive Belding’s ground squirrel ( Urocitellus beldingi ), we predicted that highly connected Sierra Nevada meadows that had warmed less or shown less precipitation change over the last century would have greater population persistence, as measured by short-term occupancy, fewer extirpations over the twentieth century, and long-term persistence measured through genetic diversity. Results Across California, U. beldingi were more likely to persist over the last century in meadows with high connectivity that were defined as refugial based on a suite of temperature and precipitation factors. In Yosemite National Park, highly connected refugial meadows were more likely to be occupied by U. beldingi . More broadly, populations inhabiting Sierra Nevada meadows with colder mean winter temperatures had higher values of allelic richness at microsatellite loci, consistent with higher population persistence in temperature-buffered sites. Furthermore, both allelic richness and gene flow were higher in meadows that had higher landscape connectivity, indicating the importance of metapopulation processes. Conversely, anthropogenic refugia, sites where populations appeared to persist due to food or water supplementation, had lower connectivity, genetic diversity, and gene flow, and thus might act as ecological traps. This study provides evidence that validates the climate change refugia concept in a contemporary context and illustrates how to integrate field observations and genetic analyses to test the effectiveness of climate change refugia and connectivity. Conclusions Climate change refugia will be important for conserving populations as well as genetic diversity and evolutionary potential. Our study shows that in-depth modeling paired with rigorous fieldwork can identify functioning climate change refugia for conservation.

California↗

USGS2008

Comparative phylogeography and population genetics within Buteo lineatus reveals evidence of distinct evolutionary lineages

Traditional subspecies classifications may suggest phylogenetic relationships that are discordant with evolutionary history and mislead evolutionary inference. To more accurately describe evolutionary relationships and inform conservation efforts, we investigated the genetic relationships and demographic histories of Buteo lineatus subspecies in eastern and western North America using 21 nuclear microsatellite loci and 375-base pairs of mitochondrial control region sequence. Frequency based analyses of mitochondrial sequence data support significant population distinction between eastern (B. l. lineatus/alleni/texanus) and western (B. l. elegans) subspecies of B. lineatus. This distinction was further supported by frequency and Bayesian analyses of the microsatellite data. We found evidence of differing demographic histories between regions; among eastern sites, mitochondrial data suggested that rapid population expansion occurred following the end of the last glacial maximum, with B. l. texanus population expansion preceding that of B. l. lineatus/alleni. No evidence of post-glacial population expansion was detected among western samples (B. l. elegans). Rather, microsatellite data suggest that the western population has experienced a recent bottleneck, presumably associated with extensive anthropogenic habitat loss during the 19th and 20th centuries. Our data indicate that eastern and western populations of B. lineatus are genetically distinct lineages, have experienced very different demographic histories, and suggest management as separate conservation units may be warranted. ?? 2008 Elsevier Inc. All rights reserved.

Molecular Phylogenetics and Evolution↗