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Robin L. Johnson

Publications and source records attributed to Robin L. Johnson.

15 recordsLinked to original sources

Population genetics of the endangered narrowly endemic Island Marble butterfly (Euchloe ausonides insulanus)

The Island Marble butterfly ( Euchloe ausonides insulanus ) is an endangered species endemic to the San Juan Islands off the coast of Washington State, United States, and British Columbia, Canada. The species was thought to be extinct for ~ 90 years before it was rediscovered at American Camp, San Juan Island National Historical Park in 1998. Here, we report the results of the first population genetic analyses for insulanus , using DNA collected non-invasively from individuals in the last known stronghold for the species. We used DNA extracted from meconium, larval exuviae, and natural mortalities to generate and test thirteen new microsatellite markers to estimate genetic diversity, population structure, and kinship. We assembled and annotated mitochondrial genomes, which were used alongside museum specimens of insulanus collected ~ 100 years ago from Vancouver Island, and other members of the E. ausonides species complex, to infer the evolutionary history of the species. The results indicated that insulanus experiences low heterozygosity, a small effective population size (N e ), and low allelic diversity. High levels of inbreeding were found in some individuals, but inbreeding was uneven across the population. No population structure or partitioning of genetic variation by host plant was detected. The mitogenomes of extant insulanus were all identical and modern samples showed a loss of allelic diversity compared to insulanus from museums. Extant insulanus formed a clade with museum specimens and we identified multiple putatively diagnostic alleles to differentiate insulanus from other subspecies. Based on these results, we outline considerations for species management and genetic monitoring.

British Columbia, Washington

Stock composition of cryptic Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) in the Restigouche River and estuary, Canada

The Atlantic sturgeon ( Acipenser oxyrinchus oxyrinchus ) is an important species in eastern North America due to its conservation status and cultural significance. Local Mi'gmaw fishers have reported an increase in sturgeon sightings over the last decade in the Restigouche River and estuary. Mi’gmaw Knowledge, oral history, and archaeological finds attest to their historical presence in the region; however, the river is not a documented habitat for Atlantic sturgeon in Western literature. Based on community interest and concern, the Gespe’gewa’gi Institute of Natural Understanding co-developed a Two-Eyed Seeing collaboration to learn more about these sturgeon. Here, we investigate their genetic origin via microsatellite analyses and hypothesized that they would originate from the closest spawning habitat, the St. Lawrence River. We found that, overall, the largest contributor to our Atlantic sturgeon sampled from the Restigouche River system was the St. Lawrence River (85.7% of samples), followed by the Wolastoq (3.6%), then a mixture of the St. Lawrence, the Wolastoq, the Kennebec, and/or the Hudson River populations (10.7%). Improving our understanding of the distribution of Atlantic sturgeon through microsatellite analyses and leveraging range-wide genetic baselines directly assesses the genetic origin of unknown stock compositions and can support the future co-management of the species.

Restigouche River and estuary

Spatiotemporal patterns in habitat use of natal and non-natal adult Atlantic sturgeon in two spawning rivers

Background Monitoring movement across an organism’s ontogeny is often challenging, particularly for long-lived or wide-ranging species. When empirical data are unavailable, general knowledge about species’ ecology may be used to make assumptions about habitat use across space or time. However, inferences about habitat use based on population-level ecology may overlook important eco-evolutionary contributions from individuals with heterogenous ethologies and could diminish the efficacy of conservation and management. Methods We analyzed over a decade of acoustic telemetry data to understand individual differences in habitat use of federally endangered adult Atlantic sturgeon ( Acipenser o. oxyrinchus ) in the Delaware and Hudson rivers during spawning season. In particular, we sought to understand whether sex or natal origin could predict patterns in habitat use, as there is a long-held assumption that adult Atlantic sturgeon seldom stray into non-natal rivers. Results In both rivers, migration timing, spawning habitat occupancy, and maximum upstream migration distance were similar between natal and non-natal individuals. While non-natal individuals represented only 13% of fish detected in the Hudson River, nearly half of all tagged fish detected in the Delaware River were non-natal and generally occupied freshwater habitats longer than natal individuals. In both systems males had more heterogenous patterns of habitat use and longer duration of occupancy than did females. Conclusions This study demonstrates the importance of non-natal rivers for fulfilling ontogenetic habitat requirements in Atlantic sturgeon. Our results may also highlight an opportunity to improve conservation and management by extending habitat designations to account for more heterogenous patterns in individual habitat use in non-natal freshwater environments.

Delaware

Integrating genetic and demographic data to refine indices of abundance for Atlantic sturgeon in the Hudson River, New York

Critical to Atlantic sturgeon Acipenser oxyrinchus oxyrinchus recovery and monitoring is the ability to estimate abundance and identify age- and stock-specific threats to survival. As adult Atlantic sturgeon spend much of their lives broadly distributed in marine and estuarine environments, it is challenging to collect data needed to estimate these demographic parameters in the adult population. Alternatively, data collected from juveniles and subadults before emigration may be used to calculate indices of abundance and provide insights into recruitment dynamics and stage-specific survival. However, uncertainty about stock mixture during early life stages may limit the use of juvenile and subadult data for monitoring recovery. To better understand early life stage stock composition, we conducted a genetic mixed-stock analysis of over 500 juvenile and subadult Atlantic sturgeon captured in an overwintering area in the Hudson River, New York, USA, from 2017 to 2022. The majority of Atlantic sturgeon in our study were natal to the Hudson River population, regardless of sex, size, or age. As such, indices of relative abundance estimated from survey data are expected to primarily characterize the demographic trends of Hudson River juvenile and subadult Atlantic sturgeon. We also found a small proportion of individuals that were most likely to have originated from more distantly located rivers, highlighting the potential for long-distance migration in juvenile and subadult Atlantic sturgeon. Results of this study strengthen our understanding of juvenile and subadult Atlantic sturgeon habitat use in the Hudson River and improve our ability to use data from early age classes to monitor recovery and stage-specific survival.

New York

Validation of a molecular sex marker in three sturgeons from eastern North America

Despite the importance of sex-specific information for sturgeon conservation and management, sex identification has been a major challenge outside of mature adults on spawning grounds. Recent work identified a sex-specific locus ( AllWSex2 ) that appears to be broadly conserved across many Acipenserids, but the assay was not validated for all species within the family. We tested the AllWSex2 marker in three sturgeon taxa (shortnose sturgeon Acipenser brevirostrum , Gulf sturgeon A. oxyrhinchus desotoi , and Atlantic sturgeon A. oxyrhinchus oxyrhinchus ) from the Atlantic and Gulf of Mexico Coasts of North America to validate its use for sex identification. Our results indicate AllWSex2 is conserved in all three taxa, presenting a new opportunity to derive sex-specific information from tissue samples, which are routinely collected from these taxa. We found high concordance (range: 97–100%) between genotypic and phenotypic/histological methods, suggesting the assay is broadly effective. However, the small amount of discordance between the methods (< 3%) suggests further refinement may be possible.

Journal of Applied Ichthyology

Genetic population assignments of Atlantic sturgeon provided to National Marine Fisheries Service, 2022

Acipenser oxyrinchus oxyrinchus (Atlantic sturgeon) were once abundant and supported large-scale fisheries throughout much of the east coast of the United States. However, historic overharvest and habitat loss resulted in dramatic declines in abundance and eventual listing under the Endangered Species Act of the United States. As part of this listing, Atlantic sturgeon populations were divided into five distinct population segments (DPSs), with many management activities occurring at the level of the DPS. However, because subadult and adult Atlantic sturgeon can make large, coast-wide migrations and often mix extensively with individuals from other populations, individuals may be exposed to conservation threats away from their natal river or DPS, ultimately making it difficult to determine the appropriate spatial scale for management activities. To help address this uncertainty, the U.S. Geological Survey performed genetic assignment tests to determine the natal origin of 329 Atlantic sturgeon that were encountered as mortalities or taken during permitted activities in 2021. Overall, most individuals assigned to the Hudson River population, with additional major contributions from the James River Fall and Delaware River populations. However, a sizeable proportion of individuals were assigned to more distantly located populations in the southeastern United States. These results highlight the prevalence of long-distance movements in Atlantic sturgeon and underscore that populations may be vulnerable to threats far from their natal rivers.

Open-File Report

Decades of global sturgeon conservation efforts are threatened by an expanding captive culture industry

After centuries of overexploitation and habitat loss, many of the world's sturgeon (Acipenseridae) populations are at the brink of extinction. Although significant resources are invested into the conservation and restoration of imperiled sturgeons, the burgeoning commercial culture industry poses an imminent threat to the persistence of many populations. In the past decade, the number and distribution of captive sturgeon facilities has grown exponentially and now encompasses diverse interest groups ranging from hobby aquarists to industrial-scale commercial facilities. Expansion of sturgeon captive culture has largely fallen outside the purview of existing regulatory frameworks, raising concerns that continued growth of this industry has real potential to jeopardize conservation of global sturgeon populations. Here, we highlight some of the most significant threats commercial culture poses to wild populations, with particular emphasis on how releases can accelerate wild population declines through mechanisms such as hybridization, introgression, competition, and disease transmission. We also note that in some circumstances, commercial captive culture has continued to motivate harvest of wild populations, potentially accelerating species' declines. Given the prevalence and trajectory of sturgeon captive culture programs, we comment on modifications to regulatory frameworks that could improve the ability of captive culture to support wild sturgeon conservation.

Fisheries Magazine

Evaluating sources of bias in pedigree-based estimates of breeding population size

Applications of genetic-based estimates of population size are expanding, especially for species for which traditional demographic estimation methods are intractable due to the rarity of adult encounters. Estimates of breeding population size ( N S ) are particularly amenable to genetic-based approaches as the parameter can be estimated using pedigrees reconstructed from genetic data gathered from discrete juvenile cohorts, therefore eliminating the need to sample adults in the population. However, a critical evaluation of how genotyping and sampling effort influence bias in pedigree reconstruction, and how these biases subsequently influence estimates of N S , is needed to evaluate the efficacy of the approach under a range of scenarios. We simulated a model system to understand the interactive effects of genotyping and sampling effort on error in genetic pedigrees reconstructed from the program COLONY . We then evaluated how errors in pedigree reconstruction influenced bias and precision in estimates of N S using three different rarefaction estimators. Results indicated that pedigree error can be minimal when adequate genetic data are available, such as when juvenile sample sizes are large and/or individuals are genotyped at many informative loci. However, even in cases for which data are limited, using results of the simulation analysis to understand the magnitude and sources of bias in reconstructed pedigrees can still be informative when estimating N S . We applied results of the simulation analysis to evaluate Nˆ S for a population of federally endangered Atlantic sturgeon ( Acipenser oxyrinchus oxyrinchus ) in the Delaware River, USA. Our results indicated that N S is likely to be three orders of magnitude lower compared with historic breeding population sizes, which is a considerable advancement in our understanding of the population status of Atlantic sturgeon in the Delaware River. Our analyses are broadly applicable in the design and interpretation of studies seeking to estimate N S and can help to guide conservation decisions when ecological uncertainty is high. The utility of these results is expected to grow as rapid advances in genetic technologies increase the popularity of genetic population monitoring and estimation.

Delaware, New Jersey, Pennsylvania

Stock composition of the historical New York Bight Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) intercept fishery revealed through microsatellite analysis of archived spines

A targeted commercial fishery for Atlantic Sturgeon Acipenser oxyrinchus oxyrinchus once operated in the New York Bight, where it was assumed that most harvested Atlantic Sturgeon were natal to the Hudson River population. However, more recent evidence suggests that the fishery may have been targeting a mixed-stock aggregation, in which case harvested Atlantic Sturgeon could have been comprised of individuals from multiple populations throughout the species’ range. Although there is now a moratorium on Atlantic Sturgeon harvest in the New York Bight, modern molecular approaches provide an opportunity to use archived tissues to perform a retrospective mixed-stock analysis on the fishery. Genomic DNA extracted from archived fin spines from 80 Atlantic Sturgeon collected nearly 30 years ago suggests that the fishery primarily harvested individuals from the Hudson River population. However, based on individual-based assignment tests, our results indicate that the fishery also harvested individuals from at least eight other populations located throughout the species’ range. This study highlights how archival hard parts that were previously used for age and growth analyses can be employed for retrospective genetic analyses. Further, because the New York Bight harbors relatively high concentrations of Atlantic Sturgeon, the study shows how localized management decisions can influence Atlantic Sturgeon conservation at rangewide scales. When integrated with more recent knowledge of species ecology, these analyses can be used to evaluate the efficacy of previous management strategies and understand the effects of historical processes on contemporary demography.

New York

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

Stock composition of Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) encountered in marine and estuarine environments on the U.S. Atlantic Coast

Atlantic sturgeon ( Acipenser oxyrinchus oxyrinchus ) is a large, anadromous fish native to the Atlantic Coast of North America. Although this species once supported important fisheries, centuries of exploitation and habitat degradation have resulted in dramatic declines, presumed extirpation in some rivers, and ultimately listing under the U.S. Endangered Species Act (ESA). Under the ESA, Atlantic sturgeon are listed as five separate Distinct Population Segments (DPSs), which form the basis for federal management. Despite state and federal protections Atlantic sturgeon still face significant threats to their recovery, including fisheries bycatch mortality, marine construction, dredging, dams, and vessel strikes. However, because subadult and adult Atlantic sturgeon migrate extensively across estuarine and marine environments and frequently form mixed-stock aggregations in non-natal habitats, it can be difficult to determine how these threats impact specific populations and DPSs. To better understand ontogenetic shifts in habitat use and stock-specific exposure to anthropogenic threats, we performed a mixed-stock analysis of 1704 Atlantic sturgeon encountered across the U.S. Atlantic Coast. Collections made north of Cape Cod, MA and south of Cape Hatteras, NC were dominated by individuals from regional stocks; however, we found extensive stock mixing in the mid-Atlantic region, particularly in coastal environments where individuals from all five DPSs were commonly observed. Subadults and adults that were encountered in offshore environments had moved, on average, 277 km from their natal source; however, 23% were sampled over 500 km from their natal river suggesting long-distance movements are relatively common in these age classes. Overall, our work highlights that Atlantic sturgeon populations are vulnerable to threats over vast areas and emphasizes the need for continued genetic monitoring to track recovery progress.

Atlantic Coast

Red Knot ( Calidris canutus ) research—Preliminary results and future opportunities

The Red Knot, Calidris canutus , is a highly migratory shorebird with a cosmopolitan distribution. Six subspecies have been identified, two of which occur regularly in North America ( C.c. rufa and C.c. roselaari ). Given their long-distance migrations through many jurisdictions and conservation status, tools are needed to reliably distinguish the subspecies when captured away from their breeding areas and to examine potential population substructure within each taxa. We used a suite of molecular approaches to develop tools to support Red Knot research and management. Although our microsatellite markers were not able to reliably distinguish C.c. rufa and C.c. roselaari , we did find evidence of population substructure within C.c. rufa .

Open-File Report

Using advanced population genomics to better understand the relationship between offshore and spawning habitat use for Atlantic Sturgeon

Atlantic Sturgeon ( Acipenser oxyrinchus oxyrinchus ) are a large-bodied anadromous fish that historically supported important fisheries along the east coast of the United States. Following years of overharvest and habitat degradation, populations experienced severe declines. In 2012, the National Marine Fisheries Service listed Atlantic Sturgeon under the Endangered Species Act (ESA; 61 FR 4722). Their listing named five Distinct Population Segments (DPSs), predicated on genetic groups composed of geographically proximate populations. Federal management of Atlantic Sturgeon presents challenges, as sturgeon from each of the five DPSs mix extensively in coastal and marine habitats yet take and recovery progress must be evaluated separately for each unit. Genetic assignment testing based on mitochondrial and microsatellite markers allows individuals to be assigned back to their natal river and DPS. However, this approach is not perfect and some individuals may be incorrectly assigned. Recent advances in genomics offer the potential of a higher resolution approach to genetic assignment testing, and thus may reduce uncertainty associated with assignment testing. In addition, genomics allows a greater number of markers to be examined from across a broader portion of the sturgeon genome, thus may provide an enhanced perspective of population structure for the species, and potentially allow other previously intractable questions to be addressed (Bernatchez et al. 2017, Supple and Shapiro 2018). We used next-generation sequencing to develop a draft genome for Atlantic Sturgeon and identify single nucleotide polymorphisms (SNPs) that could be used to resolve the natal river and DPS of individual Atlantic Sturgeon. We identified 1,210 candidate SNPs within the nuclear genome as well as 49 SNPs within the mitochondrial genome. After filtering and review, we selected 161 nuclear SNPs and 39 mitochondrial SNPs for further testing and evaluation. We used genotyping-in-thousands by sequencing (GT-seq) to simultaneously sequence nuclear SNP loci, mitochondrial SNP loci, and the existing panel of twelve microsatellite loci. This effort required a pilot sequencing run on a single sturgeon sample to test marker amplification and refine primer strengths, followed by a series of sequencing runs to generate baseline data for 288 individuals representing nine populations of Atlantic Sturgeon in four DPSs. Using baseline data from the nine populations, we ran a series of genomic analyses to characterize diversity within and among populations, providing a benchmark for this species using the new SNP markers. Allelic richness was similar for all populations, although there was a general trend of more northern population containing greater levels of allelic richness. Interestingly, we observed linkage disequilibrium among many pairs of loci within many populations. This might be the result of physical linkage but could also suggest these populations are recovering from genetic bottlenecks and/or are effectively small, leading to specific haplotypes to be favored by chance. Pairwise differentiation among populations varied among the populations ( F ST range: 0.010-0.098) and was significantly correlated ( r = 0.771; P < 0.001) to pairwise F ST observed using microsatellite markers). Population clustering and ordination techniques using the new genomic data both support an overall population structure that is similar to the current DPS management units (which were developed primarily based on microsatellite genetic data). Overall, this suggests that existing microsatellite markers and the panel of SNP markers developed in this study provide similar information about the populations structure and ecology of Atlantic Sturgeon. Given the observed differences in allele frequencies among populations, our genomic baseline supports previous assertations that Atlantic Sturgeon show natal homing, despite mixing extensively in marine waters during non-breeding periods. Lower levels of differentiation between populations in the South Atlantic DPS suggest that populations in this region may have greater levels of gene flow relative to their more northerly conspecifics, which has also previously been suggested based on microsatellite data. The observed differentiation among populations provides the necessary foundation for determining the natal river and DPS of Atlantic Sturgeon using assignment testing. We tested the utility of our new genomic baseline for resolving the population and DPS of Atlantic Sturgeon. Our nuclear SNP markers showed utility for identifying the origin of unknown Atlantic Sturgeon samples, as 86.5% were assigned to the correct DPS and 66.3% were assigned to the correct natal river. However, since this study was funded the Conservation Genetics and Genomics Laboratory at Leetown Science Center has made significant improvements to their microsatellite genetic baseline, which now performs more effectively than our new genomic approach (the genetic baseline includes 12 populations and 5 DPSs, and correctly assigns 95.8% of individuals to DPS and 84.9% of individuals to their natal population using 12 microsatellite loci). We conducted an ad hoc exploration of how additional microsatellite or nuclear SNP loci may further improve the accuracy of assignment testing. We found that additional microsatellite markers are likely to result in greater improvements in assignment efficiency than additional nuclear SNPs. However, a much larger number of SNP loci (which if identified could be sequenced using other methods that are now available; e.g., the RAD-capture approach published by Ali et al. 2016) could produce assignment efficiencies that are greater than what is currently feasible using microsatellites. In the absence of further research and development of additional SNP markers for Atlantic Sturgeon (possibly using an approach other than GT-seq), the existing microsatellite loci are the most effective means available to determine the natal river and DPS of Atlantic Sturgeon encountered in offshore waters. Because our new genomic markers were less effective than the existing panel of 12 microsatellite markers, we chose to use the existing microsatellite markers to assign Atlantic Sturgeon captured in another BOEM-funded study (cooperative agreement M16AC00003; Monitoring endangered Atlantic Sturgeon and commercial finfish habitat use offshore New York) following consultation with our project officer. Using this approach, we genotyped and assigned 186 Atlantic Sturgeon captured in coastal waters off the Rockaway Peninsula, New York. The vast majority of these sturgeon were assigned to the New York Bight DPS (94.62%), and most appear to belong to the Hudson River population (87.10%) with smaller contributions from the Delaware River population (7.53%). Smaller contributions (2.15%) were observed from six other populations, including those from the James, York, Kennebec, Ogeechee, and Edisto rivers. Although most of the fish we assigned were assigned to the nearest spawning rivers (Hudson and Delaware), the contributions from distant rivers is consistent with the propensity of this species to move long distances and form mixed stock aggregations along the continental shelf. This finding indicates that spawning populations (and their corresponding DPS) from distant locations may potentially be impacted by offshore activities. In fact, activities in this region of the New York Bight could negatively impact Atlantic Sturgeon population from at least four different DPSs. Genetic or genomic assignment testing remains an essential tool to characterize potential impacts to Atlantic Sturgeon populations and should be applied more broadly to better characterize potential impacts of activities in other locations.

Atlantic Coast

Genetic structure in the Anaxyrus boreas species group (anura, Bufonidae): an evaluation of the Southern Rocky Mountain population

The Anaxyrus boreas species group is comprised of four species endemic to the western United States: A. boreas, A. canorus, A. exsul, and A. nelsoni. Disjunct populations of the widespread western toad Anaxyrus boreas from Colorado and southern Wyoming, the southern rocky mountain population (SRMP), were previously candidates for listing under the United States Endangered Species Act (ESA) as a distinct population segment (DPS), but were removed due to a lack of significant genetic differentiation in preliminary studies. The purpose of this study was to conduct phylogeographic and population genetic analyses of A. boreas and three related species using mitochondrial DNA sequence data and nuclear microsatellite genotype data. The study is specifically focused on testing the evolutionary significance of the SRMP.

Final Report

Characterization of 13 microsatellite loci for the deep-sea coral, Lophelia pertusa (Linnaeus 1758), from the western North Atlantic Ocean and Gulf of Mexico

A suite of 13 polymorphic tri- and tetranucleotide microsatellite loci were isolated from the ahermatypic deep-sea coral, Lophelia pertusa . Among 51 individuals collected from three disjunct oceanic regions, allelic diversity ranged from six to 38 alleles and averaged 9.1 alleles per locus. Observed heterozygosity ranged from 9.1 to 96.8% and averaged 62.3% in the Gulf of Mexico population. For some loci, amplification success varied among collections, suggesting regional variation in priming site sequences. Four loci showed departures from Hardy–Weinberg equilibrium in certain collections which may reflect nonrandom mating.

Molecular Ecology Resources