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USGS2021

Genome-wide SNP analysis of three moose subspecies at the southern range limit in the contiguous United States

Genome-wide evaluations of genetic diversity and population structure are important for informing management and conservation of trailing-edge populations. North American moose ( Alces alces ) are declining along portions of the southern edge of their range due to disease, species interactions, and marginal habitat, all of which may be exacerbated by climate change. We employed a genotyping by sequencing (GBS) approach in an effort to collect baseline information on the genetic variation of moose inhabiting the species’ southern range periphery in the contiguous United States. We identified 1920 single nucleotide polymorphisms (SNPs) from 155 moose representing three subspecies from five states: A. a. americana (New Hampshire), A. a. andersoni (Minnesota), and A. a. shirasi (Idaho, Montana, and Wyoming). Molecular analyses supported three geographically isolated clusters, congruent with currently recognized subspecies. Additionally, while moderately low genetic diversity was observed, there was little evidence of inbreeding. Results also indicated > 20% shared ancestry proportions between A. a. shirasi samples from northern Montana and A. a. andersoni samples from Minnesota, indicating a putative hybrid zone warranting further investigation. GBS has proven to be a simple and effective method for genome-wide SNP discovery in moose and provides robust data for informing herd management and conservation priorities. With increasing disease, predation, and climate related pressure on range edge moose populations in the United States, the use of SNP data to identify gene flow between subspecies may prove a powerful tool for moose management and recovery, particularly if hybrid moose are more able to adapt.

Conservation Genetics↗

USGS2026

Population structure and genetic stock identification in southeastern United States loggerhead sea turtles (Caretta caretta) using genome-wide SNPs

Characterizing the genetic structure and connectivity between populations of endangered species can be used to inform management actions. In vagile species with high gene flow or recently established populations, such characterizations can be difficult to undertake using traditional genetic markers, and genetic stock identification (GSI) may be confounded by allele-sharing between populations. Loggerhead sea turtles ( Caretta caretta ) in the southeastern United States comprise seven management units (MUs) based on female philopatry inferred via mitochondrial DNA sequences, yet nuclear microsatellite data do not reflect divergence. Further, loci for accurate GSI are not currently known. To address this, we generated genome-wide single nucleotide polymorphism (SNP) data from 146 females nesting at individual sites representative of each southeastern United States MU. We found weak (F ST =0.001–0.003) but significant divergence among all MUs, with more notable divergence between the Gulf Coast and Atlantic Ocean MUs, and amongst the Atlantic Ocean MUs. We then used an iterative leave-one-out approach to identify candidate loci for GSI. This approach identified loci that could assign individuals to natal ocean basins (i.e., to the Gulf Coast or to the Atlantic Ocean), and to individual MUs within the Atlantic Ocean, with high (≥90%) success and accuracy. Analyses of genome-wide SNPs refined our understanding of the magnitude and scale of population connectivity in loggerhead turtles in the southeastern United States, and provided a foundation for the development of SNP panels for accurate, fine-scale GSI in sea turtles.

Alabama, Florida, Georgia↗

USGS2014

Next-generation genomic shotgun sequencing indicates greater genetic variability in the mitochondria of Hypophthalmichthys molitrix relative to H. nobilis from the Mississippi River, USA and provides tools for research and detection

We characterized variation within the mitochondrial genomes of the invasive silver carp ( Hypophthalmichthys molitrix ) and bighead carp ( H. nobilis ) from the Mississippi River drainage by mapping our Next-Generation sequences to their publicly available genomes. Variant detection resulted in 338 single-nucleotide polymorphisms for H. molitrix and 39 for H. nobilis . The much greater genetic variation in H. molitrix mitochondria relative to H. nobilis may be indicative of a greater North American female effective population size of the former. When variation was quantified by gene, many tRNA loci appear to have little or no variability based on our results whereas protein-coding regions were more frequently polymorphic. These results provide biologists with additional regions of DNA to be used as markers to study the invasion dynamics of these species.

Conservation Genetics Resources↗

USGS2025

Population genomics of recovery and extinction in Hawaiian honeycreepers

Native Hawaiian forest birds are experiencing an unprecedented extinction crisis. In particular, the iconic Hawaiian honeycreeper radiation has declined to just 17 out of ∼60 species remaining, most threatened with extinction due to avian malaria. Here, we investigate the genomic signatures of these declines in three honeycreeper species: the critically endangered ʻakikiki ( Oreomystis bairdi ) and ʻakekeʻe ( Loxops caeruleirostris ) and the extinct poʻouli ( Melamprosops phaeosoma ). Surprisingly, we find that Hawaiian honeycreepers, even the last known po‘ouli individual, maintain high heterozygosity compared with other island birds, reflecting historically large population sizes. This high heterozygosity may contribute to an elevated impact of inbreeding depression, as evidenced by reduced survival and reproductive success among highly inbred ‘akikiki. Demographic analysis revealed that recent precipitous declines in ‘akikiki and ‘akekeʻe coincide with the spread of avian malaria in the late 20 th century, consistent with malaria being the primary driver of population collapse. Using predictive population viability modeling, we explore potential recovery scenarios for ʻakekeʻe, which has recently declined below 100 individuals in the wild. Our models predict that, under current conditions, ‘akekeʻe is likely to go extinct in the near future. However, if mosquito control campaigns are effective at reducing malaria, recovery can still occur. These findings emphasize the urgency of ongoing mosquito control efforts, demonstrating hope for a species nearing the brink of extinction. More broadly, our study provides a detailed examination of genomic diversity, inbreeding depression, and extinction risk in a collapsing adaptive radiation, with implications for conservation of other endangered island species.

Hawaii↗

USGS2022

Genomically diverse carbapenem resistant Enterobacteriaceae from wild birds provide insight into global patterns of spatiotemporal dissemination

Carbapenem resistant Enterobacteriaceae (CRE) are a threat to public health globally, yet the role of the environment in the epidemiology of CRE remains elusive. Given that wild birds can acquire CRE, likely from foraging in anthropogenically impacted areas, and may aid in the maintenance and dissemination of CRE in the environment, a spatiotemporal comparison of isolates from different regions and timepoints may be useful for elucidating epidemiological information. Thus, we characterized the genomic diversity of CRE from fecal samples opportunistically collected from gulls ( Larus spp.) inhabiting Alaska (USA), Chile, Spain, Turkey, and Ukraine and from black kites ( Milvus migrans ) sampled in Pakistan and assessed evidence for spatiotemporal patterns of dissemination. Within and among sampling locations, a high diversity of carbapenemases was found, including Klebsiella pneumoniae carbapenemase (KPC), New Delhi metallo-beta-lactamase (NDM), oxacillinase (OXA), and Verona integron Metallo beta-lactamase (VIM). Although the majority of genomic comparisons among samples did not provide evidence for spatial dissemination, we did find strong evidence for dissemination among Alaska, Spain, and Turkey. We also found strong evidence for temporal dissemination among samples collected in Alaska and Pakistan, though the majority of CRE clones were transitory and were not repeatedly detected among locations where samples were collected longitudinally. Carbapenemase-producing hypervirulent K. pneumoniae was isolated from gulls in Spain and Ukraine and some isolates harbored antimicrobial resistance genes conferring resistance to up to 10 different antibiotic classes, including colistin. Our results are consistent with local acquisition of CRE by wild birds with spatial dissemination influenced by intermediary transmission routes, likely involving humans. Furthermore, our results support the premise that anthropogenically-associated wild birds may be good sentinels for understanding the burden of clinically-relevant antimicrobial resistance in the local human population.

Science of the Total Environment↗

USGS2015

Attenuation of monkeypox virus by deletion of genomic regions

Monkeypox virus (MPXV) is an emerging pathogen from Africa that causes disease similar to smallpox. Two clades with different geographic distributions and virulence have been described. Here, we utilized bioinformatic tools to identify genomic regions in MPXV containing multiple virulence genes and explored their roles in pathogenicity; two selected regions were then deleted singularly or in combination. In vitro and in vivo studies indicated that these regions play a significant role in MPXV replication, tissue spread, and mortality in mice. Interestingly, while deletion of either region led to decreased virulence in mice, one region had no effect on in vitro replication. Deletion of both regions simultaneously also reduced cell culture replication and significantly increased the attenuation in vivo over either single deletion. Attenuated MPXV with genomic deletions present a safe and efficacious tool in the study of MPX pathogenesis and in the identification of genetic factors associated with virulence.

Virology↗

USGS2016

Genomics reveals historic and contemporary transmission dynamics of a bacterial disease among wildlife and livestock

Whole-genome sequencing has provided fundamental insights into infectious disease epidemiology, but has rarely been used for examining transmission dynamics of a bacterial pathogen in wildlife. In the Greater Yellowstone Ecosystem (GYE), outbreaks of brucellosis have increased in cattle along with rising seroprevalence in elk. Here we use a genomic approach to examine Brucella abortus evolution, cross-species transmission and spatial spread in the GYE. We find that brucellosis was introduced into wildlife in this region at least five times. The diffusion rate varies among Brucella lineages (B3 to 8 km per year) and over time. We also estimate 12 host transitions from bison to elk, and 5 from elk to bison. Our results support the notion that free-ranging elk are currently a self-sustaining brucellosis reservoir and the source of livestock infections, and that control measures in bison are unlikely to affect the dynamics of unrelated strains circulating in nearby elk populations.

Nature Communications↗

USGS2021

Activity-based, genome-resolved metagenomics uncovers key populations and pathways involved in subsurface conversions of coal to methane

Microbial metabolisms and interactions that facilitate subsurface conversions of recalcitrant carbon to methane are poorly understood. We deployed an in situ enrichment device in a subsurface coal seam in the Powder River Basin (PRB), USA, and used BONCAT-FACS-Metagenomics to identify translationally active populations involved in methane generation from a variety of coal-derived aromatic hydrocarbons. From the active fraction, high-quality metagenome-assembled genomes (MAGs) were recovered for the acetoclastic methanogen, Methanothrix paradoxum , and a novel member of the Chlorobi with the potential to generate acetate via the Pta-Ack pathway. Members of the Bacteroides and Geobacter also encoded Pta-Ack and together, all four populations had the putative ability to degrade ethylbenzene, phenylphosphate, phenylethanol, toluene, xylene, and phenol. Metabolic reconstructions, gene analyses, and environmental parameters also indicated that redox fluctuations likely promote facultative energy metabolisms in the coal seam. The active “ Chlorobi PRB” MAG encoded enzymes for fermentation, nitrate reduction, and multiple oxygenases with varying binding affinities for oxygen. “ M. paradoxum PRB” encoded an extradiol dioxygenase for aerobic phenylacetate degradation, which was also present in previously published Methanothrix genomes. These observations outline underlying processes for bio-methane from subbituminous coal by translationally active populations and demonstrate activity-based metagenomics as a powerful strategy in next generation physiology to understand ecologically relevant microbial populations.

Montana, Wyoming↗

USGS2010

Complete mitochondrial genome of a Pleistocene jawbone unveils the origin of polar bear

The polar bear has become the flagship species in the climate-change discussion. However, little is known about how past climate impacted its evolution and persistence, given an extremely poor fossil record. Although it is undisputed from analyses of mitochondrial (mt) DNA that polar bears constitute a lineage within the genetic diversity of brown bears, timing estimates of their divergence have differed considerably. Using next-generation sequencing technology, we have generated a complete, high-quality mt genome from a stratigraphically validated 130,000- to 110,000-year-old polar bear jawbone. In addition, six mt genomes were generated of extant polar bears from Alaska and brown bears from the Admiralty and Baranof islands of the Alexander Archipelago of southeastern Alaska and Kodiak Island. We show that the phylogenetic position of the ancient polar bear lies almost directly at the branching point between polar bears and brown bears, elucidating a unique morphologically and molecularly documented fossil link between living mammal species. Molecular dating and stable isotope analyses also show that by very early in their evolutionary history, polar bears were already inhabitants of the Artic sea ice and had adapted very rapidly to their current and unique ecology at the top of the Arctic marine food chain. As such, polar bears provide an excellent example of evolutionary opportunism within a widespread mammalian lineage.

PNAS↗

USGS2024

Genomic characterization of highly pathogenic H5 avian influenza viruses from Alaska during 2022 provides evidence for genotype-specific trends of spatiotemporal and interspecies dissemination

The ongoing panzootic of highly pathogenic H5 clade 2.3.4.4b avian influenza (HPAI) spread to North America in late 2021, with detections of HPAI viruses in Alaska beginning in April 2022. HPAI viruses have since spread across the state, affecting many species of wild birds as well as domestic poultry and wild mammals. To better understand the dissemination of HPAI viruses spatiotemporally and among hosts in Alaska and adjacent regions, we compared the genomes of 177 confirmed HPAI viruses detected in Alaska during April – December 2022. Results suggest multiple viral introductions into Alaska between November 2021 and August or September 2022, as well as dissemination to areas within and outside of the state. Viral genotypes differed in their spatiotemporal spread, likely influenced by timing of introductions relative to population immunity. We found evidence for dissemination of HPAI viruses between wild bird species, wild birds and domestic poultry, as well as wild birds and wild mammals. Continued monitoring for and genomic characterization of HPAI viruses in Alaska can improve our understanding of the evolution and dispersal of these economically costly and ecologically relevant pathogens.

Emerging Microbes & Infections↗

USGS2018

The complete mitochondrial genome of Hine’s emerald dragonfly (Somatochlora hineana Williamson) via NGS sequencing

Here, we report the complete mitochondrial genome of the endangered Hine’s emerald dragonfly (HED), Somatochlora hineana Williamson. Data were generated via next generation sequencing (NGS) and assembled using a mitochondrial baiting and iterative mapping approach. The full length circular genome is 15,705 bp with 26.6% GC content. It contains the typical metazoan set of 37 genes: 13 protein-coding genes, 22 transfer RNA (tRNA) and 2 ribosomal RNA (rRNA) genes, and an A + T-rich control region. To our knowledge, this is the first report of the complete HED mitogenome.

Mitochondrial DNA Part B↗

USGS2018

The complete maternal mitochondrial genome sequences of two imperiled North American freshwater mussels: Alasmidonta heterodon and Alasmidonta varicosa (Bivalvia: Unionoida: Unionidae)

The freshwater mussels Alasmidonta heterodon and A. varicosa historically inhabited rivers along the North American Atlantic coast from the Carolinas, U.S.A., to New Brunswick, CA. However, many populations have been extirpated, and A. heterodon is now federally listed in the U.S.A. as endangered, and both A. heterodon and A. varicosa are listed as vulnerable on the IUCN Red List. To facilitate genetic study of these species, we sequenced the complete female mitochondrial genomes of A. heterodon (15,909 bp; GenBank accession no. MG905826), and A. varicosa (15,693 bp; GenBank accession no. MG938673). Both mitogenomes contained 14 protein coding genes, 2 rRNA genes, and 22 tRNAs with the same gene order as reported for other members of the subfamily Anodontinae. When these two genomes were put into a phylogenetic context with other members of the Unionidae, they clustered together with other species in the subfamily Anodontinae, Tribe Anodontini.

Mitochondrial DNA Part B↗

USGS1999

Low abundance of microsatellite repeats in the genome of the brown-headed cowbird (Molothrus ater)

A cosmid library made from brown-headed cowbird ( Molothrus ater ) DNA was examined for representation of 17 distinct microsatellite motifs including all possible mono-, di-, and trinucleotide microsatellites, and the tetranucleotide repeat (GATA) n . The overall density of microsatellites within cowbird DNA was found to be one repeat per 89 kb and the frequency of the most abundant motif, (AGC) n , was once every 382 kb. The abundance of microsatellites within the cowbird genome is estimated to be reduced approximately 15-fold compared to humans. The reduced frequency of microsatellites seen in this study is consistent with previous observations indicating reduced numbers of microsatellites and other interspersed repeats in avian DNA. In addition to providing new information concerning the abundance of microsatellites within an avian genome, these results provide useful insights for selecting cloning strategies that might be used in the development of locus-specific microsatellite markers for avian studies.

Journal of Heredity↗

USGS2021

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↗

USGS2018

Ecological genomics predicts climate vulnerability in an endangered southwestern songbird

Few regions have been more severely impacted by climate change in the USA than the Desert Southwest. Here, we use ecological genomics to assess the potential for adaptation to rising global temperatures in a widespread songbird, the willow flycatcher ( Empidonax traillii ), and find the endangered desert southwestern subspecies ( E. t. extimus ) most vulnerable to future climate change. Highly significant correlations between present abundance and estimates of genomic vulnerability – the mismatch between current and predicted future genotype–environment relationships – indicate small, fragmented populations of the southwestern willow flycatcher will have to adapt most to keep pace with climate change. Links between climate‐associated genotypes and genes important to thermal tolerance in birds provide a potential mechanism for adaptation to temperature extremes. Our results demonstrate that the incorporation of genotype–environment relationships into landscape‐scale models of climate vulnerability can facilitate more precise predictions of climate impacts and help guide conservation in threatened and endangered groups.

Ecology Letters↗

USGS2019

Parallel signatures of selection at genomic islands of divergence and the major histocompatibility complex in ecotypes of sockeye salmon across Alaska

Understanding the genetic mechanisms that facilitate adaptive radiation is an important component of evolutionary biology. Here, we genotyped 82 neutral SNPs, seven SNPs in islands of divergence identified in a previous study (island SNPs), and a region of the major histocompatibility complex (MHC) in 32 populations of sockeye salmon to investigate whether conserved genes and genomic regions are involved in adaptive radiation. Populations representing three ecotypes were sampled from seven drainages with differing habitats and colonization histories spanning a range of 2,000 km. We found strong signatures of parallel selection across drainages at the island SNPs and MHC, suggesting that the same loci undergo divergent selection during adaptive radiation. However, patterns of differentiation at most island SNPs and the MHC were not associated with ecotypes, suggesting that these loci are responding differently to a mosaic of selective pressures. Our study provides some of the first evidence that conserved genomic islands may be involved in adaptive divergence of salmon populations. Additionally, our data provide further support for the hypothesis that sockeye salmon inhabiting rivers unconnected to lakes harbour similar genetic diversity across large distances, are likely the ancestral form of the species, and have repeatedly recolonized lake systems as they have become available after glacial recession. Finally, our results highlight the value and importance of validating outlier loci by screening additional populations and regions, a practice that will hopefully become more common in the future.

Alaska↗

USGS2021

Harnessing landscape genomics to identify future climate resilient genotypes in a desert annual

Local adaptation features critically in shaping species responses to changing environments, complicating efforts to revegetate degraded areas. Rapid climate change poses an additional challenge that could reduce fitness of even locally sourced seeds in restoration. Predictive restoration strategies that apply seeds with favourable adaptations to future climate may promote long‐term resilience. Landscape genomics is increasingly used to assess spatial patterns in local adaption and may represent a cost‐efficient approach for identifying future‐adapted genotypes. To demonstrate such an approach, we genotyped 760 plants from 64 Mojave Desert populations of the desert annual Plantago ovata . Genome scans on 5,960 SNPs identified 184 potentially adaptive loci related to climate and satellite vegetation metrics. Causal modelling indicated that variation in potentially adaptive loci was not confounded by isolation by distance or isolation by habitat resistance. A generalized dissimilarity model (GDM) attributed spatial turnover in potentially adaptive loci to temperature, precipitation and NDVI amplitude, a measure of vegetation green‐up potential. By integrating a species distribution model (SDM), we find evidence that summer maximum temperature may both constrain the range of P. ovata and drive adaptive divergence in populations exposed to higher temperatures. Within the species’ current range, warm‐adapted genotypes are predicted to experience a fivefold expansion in climate niche by midcentury and could harbour key adaptations to cope with future climate. We recommend eight seed transfer zones and project each zone into its relative position in future climate. Prioritizing seed collection efforts on genotypes with expanding future habitat represents a promising strategy for restoration practitioners to address rapidly changing climates.

California, Nevada↗

USGS2022

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↗