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

White, Shannon L.; Kazyak, David C.; Darden, Tanya L.; Farrae, Daniel J.; Lubinski, Barbara A.; Johnson, Robin L.; Eackles, Michael S.; Balazik, Matthew T.; Brundage, Harold M.; Fox, Adam G.; Fox, Dewayne A.; Hager, Christian H.; Kahn, Jason E.; Wirgin, Isaac I.
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.
SCOPUS:85111798968
ISSN: 1566-0621
CID: 5001482

Toxic Effects of Polychlorinated Biphenyl Congeners and Aroclors on Embryonic Growth and Development

Singleman, Corinna; Zimmerman, Alison; Harrison, Elise; Roy, Nirmal K; Wirgin, Isaac; Holtzman, Nathalia G
Polychlorinated biphenyls (PCBs) cause significant health and reproductive problems in many vertebrates. Exposure during embryogenesis likely leads to defects in organ development, compromising survival and growth through adulthood. The present study identifies the impact of PCBs on the embryonic development of key organs and resulting consequences on survival and growth. Zebrafish embryos were treated with individual PCB congeners (126 or 104) or one of 4 Aroclor mixtures (1016, 1242, 1254, or 1260) and analyzed for changes in gross embryonic morphology. Specific organs were assessed for defects during embryonic development, using a variety of transgenic zebrafish to improve organ visualization. Resulting larvae were grown to adulthood while survival and growth were assayed. Embryonic gross development on PCB treatment was abnormal, with defects presenting in a concentration-dependent manner in the liver, pancreas, heart, and blood vessel organization. Polychlorinated biphenyl 126 treatment resulted in the most consistently severe and fatal phenotypes, whereas treatments with PCB 104 and Aroclors resulted in a range of more subtle organ defects. Survival of fish was highly variable although the growth rates of surviving fish were relatively normal, suggesting that maturing PCB-treated fish that survive develop compensatory strategies needed to reach adulthood. Life span analyses of fish from embryogenesis through adulthood, as in the present study, are scarce but important for the field because they help identify foci for further studies. Environ Toxicol Chem 2020;00:1-15. © 2020 SETAC.
PMID: 33118622
ISSN: 1552-8618
CID: 4712352

Atlantic Coastwide Population Structure of Striped Bass Morone saxatilis Using Microsatellite DNA Analysis

Wirgin, Isaac; Maceda, Lorraine; Tozer, Matt; Stabile, Joseph; Waldman, John
Striped bass Morone saxatilis support one of the most popular and important inshore recreational and commercial fisheries along the Atlantic Coast of North America. Populations at both extremes of its distribution are largely resident while those in the center of its range (Hudson River, New York, to Roanoke River, North Carolina) are seasonally migratory, ranging from the Bay of Fundy, Canada, to the Outer Banks of North Carolina. Historically, population abundances of striped bass fluctuated widely, sometimes resulting in the imposition of severe management measures to restrict their harvest. Detailed knowledge of its rangewide population structure would aid in more effective management; however, most genetic studies addressing the structure of the migratory coastal stock have largely failed to achieve this goal. To address this need, we used multi-loci microsatellite DNA analysis. We identified six genetically distinct populations across the species' distribution, including the Miramichi, Shubenacadie, Hudson, Delaware-Chesapeake, Roanoke, and Santee-Cooper rivers. We also report significant genetic differentiation between the Nanticoke and Choptank rivers along the eastern shore of the Chesapeake Bay and collections from tributaries along the western shore of the Bay. The Annapolis and Saint John rivers, tributaries of the Bay of Fundy, historically hosted striped bass aggregations that were extirpated, or nearly so, by anthropogenic stressors in the late 20th century. No specimens with unique genotypes were found in collections from either river; instead the vast majority were admixed with genotypes of Shubenacadie River, Hudson River, Chesapeake Bay, and Roanoke River lineage. Finally, we show in simulations that these genetic markers should be informative in quantifying the contributions of the Hudson River, Chesapeake Bay-Delaware, and Roanoke River to mixed-stock harvests that occur within the range of the coastal migratory stock.
PMCID:8726014
PMID: 34987272
ISSN: 0165-7836
CID: 5110802

Population genetic assessment of anadromous and resident striped bass (Morone saxatilis) in the roanoke river system, Eastern United States

Harris, Sheila C.; Cope, W. Robert; Wirgin, Isaac; Hallerman, Eric M.
Striped bass is the subject of important commercial and sport fisheries in North America. The Roanoke River drainage"”especially Smith Mountain Lake, Leesville Lake, and Kerr Reservoir"”has popular recreational striped bass fisheries. After construction of five hydroelectric dams, populations became landlocked, declined, and have been supplemented by stocking. A key basis for responsibly augmenting populations is to characterize genetic variation and incorporate the findings into responsible hatchery and stocking practices. Genetic variation at 12 microsatellite DNA loci was evaluated among 837 striped bass representing 16 collections across the native range; populations from rivers in South Carolina, North Carolina, Chesapeake Bay, and Hudson River were screened to provide context for assessing genetic structure within the Roanoke system. Analysis of population genetic differentiation showed landlocked Roanoke River striped bass to be distinctive. Subject to genetic isolation, high M ratios, and relatively low Ne estimates suggest loss of genetic variation, and relatedness analysis showed heightened frequencies of related individuals. These insights into population genetics, demographics, and existing guidelines for broodstock acquisition and mating designs can inform genetically cognizant hatchery management and stocking for striped bass in the Roanoke River drainage. In particular, we recommend the use of larger numbers of breeders and factorial mating designs to increase the genetic diversity of propagated striped bass stocked within the Roanoke River drainage.
SCOPUS:85090653848
ISSN: 2410-3888
CID: 4612962

Use of social network analysis to examine preferential co-occurrences in Atlantic Sturgeon Acipenser oxyrinchus oxyrinchus Mitchill, 1815

Lilly, Jessie; McLean, Montana F.; Dadswell, Michael J.; Wirgin, Isaac; Comolli, Perry; Stokesbury, Michael J.W.
Background: Application of Social Network Analysis (SNA) to acoustic telemetry is a useful approach to examine social behavior in fish. Atlantic Sturgeon (Acipenser oxyrinchus oxyrinchus) are ancient, long-lived anadromous finfish. Although Atlantic Sturgeon have been the subject of numerous telemetry studies, none have used SNA to analyze their co-occurrence behavior. During 2010-2014 Atlantic Sturgeon (n = 103) that were later genetically identified as being from the Saint John River, Canada and the Kennebec River, US were captured by otter trawl and brush weir in Minas Basin, Bay of Fundy, Canada, and acoustically tagged. Using data from moored acoustic receivers within foraging habitat in Minas Basin, we tested if Atlantic Sturgeon formed social associations that were random or structured during 2012 to 2014; and whether these co-occurrences consisted of individuals from the same river of origin or capture date. Results: Irrespective of genetic origin and initial capture date, Atlantic Sturgeon formed co-occurrences in Minas Basin that were significantly different than would be observed by chance during 2012 and very close to significant during 2013. Analysis demonstrated that some Atlantic Sturgeon preferentially co-occur within their primary feeding habitat. Conclusions: The current threats to Atlantic Sturgeon aggregations within the Bay of Fundy, Nova Scotia, include bycatch in fisheries throughout their coastal migration routes and more recently the development of tidal turbines along their migratory corridor to their summer aggregation site. It is important to determine if Atlantic Sturgeon form aggregations with conspecifics from the same population to inform management decisions regarding threats to groups of individuals. This study indicated that Atlantic Sturgeon may form preferential co-occurrences within their feeding aggregation and co-occurrences that were identified were not dependent upon population of origin or initial capture date.
SCOPUS:85085090236
ISSN: 2050-3385
CID: 4463802

Contemporary and historical effective population sizes of Atlantic sturgeon Acipenser oxyrinchus oxyrinchus

Waldman, John; Alter, S. Elizabeth; Peterson, Douglas; Maceda, Lorraine; Roy, Nirmal; Wirgin, Isaac
Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) is an anadromous fish of considerable conservation concern, following its long history of overfishing and exposure to a variety of other anthropogenic stressors. Though reaching a large size, population abundances (Nc) of Atlantic sturgeon are not easily surveyed using traditional fishery methods because of their relative scarcity and their many age classes, often exhibiting extensive and differential movements that render them not readily amenable to traditional sampling efforts. A metric of their vulnerability to inbreeding and a possible alternative to Nc for abundance monitoring is effective population size (Ne). We surveyed 14 Atlantic sturgeon populations across their range using a suite of DNA microsatellite markers. Contemporary levels of Ne ranged from 1 in the St. Marys River, Florida-Georgia, to 156 in the Hudson River, New York. Historical Ne estimates averaged about 11.5xhigher than contemporary estimates, with a high of 927 for the Kennebec River population. Because of a mix of life history characteristics that make traditional Ne estimates based on imperfectly mixed year classes of juveniles questionable, we propose and provide results ofa new, more robust and diagnostic approach based on sequential cohorts, termed Ne Max. Although contemporary Ne values obtained were at levels that might be considered troublesome, we suggest that the unique life history factors of this species may render it more resistant than other taxa to inbreeding effects. Because of the many differences among populations in size, age, and sex ratio and in harvest histories, we do not believe that a reliable extrapolation factor between Ne and Nc is yet possible. However, ongoing monitoring of Ne and Nc in populations might be sensitive to population changes and could form the basis of determining a relationship between Ne and Nc.
ISI:000462207000003
ISSN: 1566-0621
CID: 3796792

Occurrence of Atlantic Sturgeon in the St. Marys River, Georgia

Fox, Adam G.; Wirgin, Isaac I.; Peterson, Douglas L.
The Atlantic Sturgeon Acipenser oxyrinchus oxyrinchus is an anadromous species that historically has been found along the Atlantic coast of North America from maritime Canada to the St. Johns River, Florida. Decades of overharvest and habitat loss has resulted in range-wide population declines, and in 2012 the species was listed under the U.S. Endangered Species Act as five Distinct Population Segments (DPSs). The extirpation of several populations, including some in the South Atlantic DPS, was identified as an important consideration in the final determination to list this DPS as endangered. In the St. Marys River, Georgia, the second-most southern river within their historical range, Atlantic Sturgeon were thought to have been extirpated for several decades. The objectives of this study were to document the seasonal occurrence of Atlantic Sturgeon in the St. Marys River and to document any evidence of an extant population in the river. During the summers of 2013-2016, we set 533 nets and captured a total of 25 Atlantic Sturgeon, including several age-1, river-resident juveniles. Genetic analyses indicated that these juveniles were descendants of a remnant population that is distinct but more closely related to other populations within the South Atlantic DPS than those in more northern rivers. Using acoustic telemetry, we monitored the movements and habitat use of 14 individual sturgeon in the St. Marys River estuary. Acoustically tagged juveniles resided mainly within the St. Marys River main stem, but we did detect a number of adult migrants using Cumberland Sound on a seasonal basis. Our results indicate that Atlantic Sturgeon persist in the St. Marys River and that the estuary also provides seasonally important habitat for migrating adults from other populations.
ISI:000454411800007
ISSN: 1942-5120
CID: 3574372

Characterization of AHR1 and its functional activity in Atlantic sturgeon and shortnose sturgeon

Roy, Nirmal K; DellaTorre, Melissa; Candelmo, Allison; Chambers, R Christopher; Habeck, Ehren; Wirgin, Isaac
Sturgeon species are imperiled world-wide by a variety of anthropogenic stressors including chemical contaminants. Atlantic sturgeon, Acipenser oxyrinchus, and shortnose sturgeon, Acipenser brevirostrum, are largely sympatric acipenserids whose young life-stages are often exposed to high levels of benthic-borne PCBs and PCDD/Fs in large estuaries along the Atlantic Coast of North America. In previous laboratory studies, we demonstrated that both sturgeon species are sensitive to early life-stage toxicities from exposure to environmentally relevant concentrations of coplanar PCBs and TCDD. The sensitivity of young life-stages of fishes to these contaminants varies among species by three orders of magnitude and often is due to variation in the structure and function of the aryl hydrocarbon receptor (AHR) pathway. Unlike mammals, fishes have two forms of AHR (AHR1 and AHR2) with AHR2 usually being more highly expressed across tissues and functional in mediating toxicities. Based on previous studies in white sturgeon, A. transmontanus, we hypothesized that sturgeon taxa are unusually sensitive to these contaminants because of higher levels of expression and functional activity of AHR1 than in other fish taxa. To address this possibility, we characterized AHR1 in both Atlantic Coast sturgeon species, evaluated its' in vivo expression in young life-stages and in multiple tissues of shortnose sturgeon, and tested its ability to drive reporter gene expression in AHR-deficient cells treated with graded doses of PCB126 and TCDD. Similar to white sturgeon and lake sturgeon, AHR1 amino acid sequences in Atlantic sturgeon and shortnose sturgeon were more similar to mammalian AHRs and avian AHR1s than to AHR1 in other fishes, suggesting their greater functionality in sturgeon species than in other fishes. Exposure to graded doses of coplanar PCBs and TCDD usually failed to significantly induce AHR1 expression in young life-stages or most tissues of shortnose sturgeon. However, in reporter gene assays, AHR1 drove higher levels of gene expression than AHR2 alone, but their binary combination failed to drive higher levels of expression than either AHR alone. In total, our results suggest that AHR1 may be more functional in sturgeon species than in other fishes, but probably does not explain their heightened sensitivity to these contaminants.
PMID: 30312899
ISSN: 1879-1514
CID: 3335162

DPS and population origin of subadult Atlantic Sturgeon in the Hudson River

Wirgin, Isaac; Roy, Nirmal K.; Maceda, Lorraine; Mattson, Mark T.
Atlantic Sturgeon Acipenser oxyrinchus oxyrinchus is listed under the U.S. Endangered Species Act as five Distinct Population Segments (DPS). Subadult Atlantic Sturgeon are highly migratory in coastal waters and often move to non-natal estuaries where they encounter a variety of anthropogenic disturbances that may compromise their survival. The Hudson River estuary hosts large numbers of subadult Atlantic Sturgeon seasonally, but their DPS and population origin is unknown. We used microsatellite DNA analysis at 11 loci and sequence analysis of the mitochondrial DNA control region in Individual Based Assignment testing to determine the origin of 148 sub adult Atlantic Sturgeon that were collected in the tidal Hudson River estuary between river kilometers (RKM)5 and RKM 124 north of the Battery in New York City (RKM 0). We also determined the origin of eight dead specimens (subadults and adults) that were likely victims of vessel strikes and found floating between RKM27 and RKM60. We determined that 142 of 148 subadults assigned to the Hudson River (New York Bight DPS), the vast majority (138 of 142) with at least 95%, and usually, 100%, probability. All eight dead specimens assigned to the Hudson River with greater than 99% probability. Of the six subadult specimens that did not assign to the Hudson, two each assigned to the Kennebec River (Gulf of Maine DPS) and Delaware River (New York Bight DPS), one to the Ogeechee River (South Atlantic DPS), and one to the James River (Chesapeake Bay DPS). Our analysis allows the effects of anthropogenic threats in the Hudson River to be apportioned to the DPS and natal river populations of Atlantic Sturgeon found there and serves as a model for genetic population composition analysis for subadult Atlantic Sturgeon in other impacted estuaries.
ISI:000442059900018
ISSN: 0165-7836
CID: 3260872

Satellite driven distribution models of endangered Atlantic sturgeon occurrence in the mid-Atlantic Bight

Breece, Matthew W.; Fox, Dewayne A.; Haulsee, Danielle E.; Wirgin, Isaac I.; Oliver, Matthew J.
Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) is an endangered species that migrate through, and occupy the coastal waters of the mid-Atlantic Bight where they interact with anthropogenic activities. Measures to understand and avoid Atlantic sturgeon that take into consideration the dynamic nature of their habitat may reduce harmful interactions. In this study, we matched fisheries independent biotelemetry observations of Atlantic sturgeon with daily satellite observations to construct a time resolved spatial distribution model of Atlantic sturgeon. We determined that depth, day-of-year, sea surface temperature, and light absorption by seawater were the most important predictors of Atlantic sturgeon occurrence. Demographic factors, such as sex and river-of-origin were of secondary importance. We found strong spatial differences in spring and fall migration patterns, when anthropogenic interactions peak. Our cross-validated models correctly identified > 88% of biotelemetry observations in our study region. Our models also correctly identified similar to 64% of bycatch observations throughout the year. However, during their migrations, when harmful interactions were highest, our models correctly identified similar to 90% of fisheries dependent observations. We suggest that this model can be used for guidance to managers and stakeholders to reduce interactions with this highly imperiled species, thereby enhancing conservation and recovery efforts.
ISI:000429491500011
ISSN: 1054-3139
CID: 3049332