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Hapeman, P., E. K. Latch, O. E. Rhodes, B. J. Swanson, and C. W. Kilpatrick. 2017. Genetic population structure of fishers (Pekania pennanti) in the Great Lakes region: remnants and reintroductions. Canadian Journal of Zoology 95: 869-876.

Abstract:
Reintroduction programs have been pivotal in augmenting populations of fishers (Pekania pennanti (Erxleben, 1777)) and re-establishing them to their former range in North America. The majority of reintroduction efforts in fishers have been considered demographically successful, but reintroductions can alter genetic population structure and success has rarely been evaluated in fishers from a genetic standpoint. We used microsatellite data (n = 169) to examine genetic population structure of fishers in the Great Lakes region and comment on the success of past reintroductions at two different spatial scales. We found significant genetic population structure among source and reintroduced populations within the Great Lakes region and largescale genetic structure between fisher populations located in two geographically distant regions (Great Lakes and Northeast) in the eastern United States. Reintroductions associated with the Great Lakes produced results that were largely consistent with other studies of fisher reintroductions in the Northeast. However, our data are the first to support a measurable impact on genetic population structure in Pekania pennanti pennanti (Erxleben, 1777) from a reintroduction using geographically distant source and reintroduced populations. When feasible, we strongly recommend that reintroduction programs include an investigation of the underlying genetic structure to better define intended goals and supplement measures of demographic success.


Hoffman, J. R., J. R. Willoughby, B. J. Swanson, K. L. Pangle, and D. T. Zanatta. 2017. Detection of barriers to dispersal is masked by long lifespans and large population sizes Ecology and Evolution DOI: 10.1002/ece3.3470

Abstract:
Population genetic analyses of species inhabiting fragmented landscapes are essential tools for conservation. Occasionally, analyses of fragmented populations find no evidence of isolation, even though a barrier to dispersal is apparent. In some cases, not enough time may have passed to observe divergence due to genetic drift, a problem particularly relevant for long-lived species with overlapping generations. Failing to consider this quality during population structure analyses could result in incorrect conclusions about the impact of fragmentation on the species. We designed a model to explore how lifespan and population size influence perceived population structure of isolated populations over time. This iterative model tracked how simulated populations of variable lifespan and population size were affected by drift alone, using a freshwater mussel, Quadrula quadrula (mapleleaf), as a model system. In addition to exhibiting dramatic lifespan variability among species, mussels are also highly imperiled and exhibit fragmentation by dams throughout the range of many species. Results indicated that, unless population size was small (<50 individuals) or lifespan short (<22 years), observing genetic divergence among populations was unlikely. Even if wild populations are isolated, observing population structure in long-lived mussels from modern damming practices is unlikely because it takes longer for population structure to develop in these species than most North American dams have existed. Larger population sizes and longer lifespans increase the time needed for significant divergence to occur. This study helps illuminate the factors that influence genetic responses by populations to isolation and provides a useful model for conservation-oriented research. This study highlights the importance of long-term genetic monitoring of reintroduced populations.


Sattler, S. L., J. R. Willoughby, and B. J. Swanson. 2017. Decline of heterozygosity in a large but isolated population: a 45-year examination of moose genetic diversity on Isle Royale. PeerJ DOI 10.7717/peerj.3584

Abstract:
Wildlife conservation and management approaches typically focus on demographic measurements to assess population viability over both short and long periods. However, genetic diversity is an important predictor of long term population vitality. We investigated the pattern of change in genetic diversity in a large and likely isolated moose (Alces alces) population on Isle Royale (Lake Superior) from 1960-2005. We characterized samples, partitioned into five different 5-year periods, using nine microsatellite loci and a portion of the mtDNA control region. We also simulated the moose population to generate a theoretical backdrop of genetic diversity change. In the empirical data, we found that the number of alleles was consistently low and that observed heterozygosity notably declined from 1960 to 2005 (p = 0.08, R2= 0.70). Furthermore, inbreeding coefficients approximately doubled from 0.08 in 1960-1965 to 0.16 in 2000-2005. Finally, we found that the empirical rate of observed heterozygosity decline was faster than the rate of observed heterozygosity loss in our simulations. Combined, these data suggest that genetic drift and inbreeding occurred in the Isle Royale moose populations over the study period, leading to significant losses in heterozygosity. Although inbreeding can be mitigated by migration, we found no evidence to support the occurrence of recent migrants into the population using analysis of ourmtDNAhaplotypes nor microsatellite data. Therefore, the Isle Royale moose population illustrates that even large populations are subjected to inbreeding in the absence of migration. This study highlights the importance of long-term genetic monitoring of reintroduced populations.


Hillman, T. L., P. Keenlance, J. A. Moore, B. J. Swanson, J. J. Jacquot, J. C. Witt, and A. Cornman. 2017. Genetic diversity of reintroduced American martens in Michigan's Lower Peninsula. Journal of Mammalogy 98:1487 - 1496.

Abstract:
Reintroductions are an important conservation and management technique used to restore extirpated populations. Negative genetic consequences (e.g., diversity loss, bottlenecks, inbreeding) are often an unintentional result of reintroductions, due to a small number of founders or suboptimal habitat at release sites. American martens (Martes americana) were extirpated from Michigan's Lower Peninsula in 1911 due to habitat loss and unregulated trapping. Martens were reintroduced into 2 areas of the Lower Peninsula in 1985 - 1986. The Lower Peninsula reintroduction was characterized by a relatively small number of founders (85 individuals) released into 2 geographically disparate, fragmented sites. We genotyped martens sampled at the 2 release sites approximately 20 - 25 years since reintroduction, using 11 microsatellite loci. We detected low average allelic richness (3.92 alleles per locus), moderate levels of inbreeding (mean FIS = 0.106), and multiple loci with significant heterozygote deficiencies. Effective population size estimates were small, ranging between 6 and 27 individuals depending on the estimator and the sample group. We also detected significant population structuring between the release sites (FST = 0.093 using the most recent sample). With small population size and limited to no gene flow, we predict the 2 Lower Peninsula marten populations will continue to diverge and potentially further lose genetic diversity. This study highlights the importance of long-term genetic monitoring of reintroduced populations.


Ellison, S. A., and B. J. Swanson. 2016. Individual Identification of Raccoons (Procyon lotor) Using Track Plate Foot Printing American Midland Naturalist 176: 306 - 312

Abstract:
Population studies are widely used in conservation and management efforts, but acquiring necessary data sets can be difficult. Convenience sampling or camera monitoring may result in biased outcomes, while explicit approaches such as genetic analysis may be impractical due to cost and time. Traditional mark recapture methods are frequently intrusive and pose risk to both animals and handlers that could lead to mortality. These factors highlight the need for a simple, inexpensive, and non-invasive approach to assess species density. One possible technique which addresses these issues is track plate footprinting. We collected raccoon (Procyon lotor) footprints and examined the ability to distinguish individuals by their metacarpal pads from a 225 ha reserve. The probability of identity (PID) for back right feet ranged from 5.72x10-9 to 6.71x10-12 and from 3.34x10-8 to 3.55x10-10 for the back left feet, indicating that it was unlikely any two raccoons shared the same papillae pattern. The minimum number of raccoons known to be alive was estimated to be 12 to 17 individuals depending upon the foot and scale of resolution used, with estimates from program the Capture ranging from 34 to 38 raccoons. Our results show that track plate footprint can be used to unambiguously identify individual raccoons, may be useful in mark-recapture studies, and is likely to be applicable to other species with large pads.


Rico, Y., D. M., Ethier, C. M. Davy, J. Sayers, R. D. Weir, B. J. Swanson, J. J. Nocera, and C. J. Kyle 2016. Spatial patterns of immunogenetic and neutral variation underscore the conservation value of small, isolated American badger populations. Evolutionary Applications DOI: 10.1111/eva.12410

Abstract:
Small and isolated populations often exhibit low genetic diversity due to drift and inbreeding, but may simultaneously harbour adaptive variation. We investigate spatial distributions of immunogenetic variation in American badger subspecies (Taxidea taxus), as a proxy for evaluating their evolutionary potential across the northern extent of the species' range. We compared genetic structure of 20 microsatellites and the major histocompatibility complex (MHC DRB exon 2) to evaluate whether small, isolated populations show low adaptive polymorphism relative to large and well-connected populations. Our results suggest that gene flow plays a prominent role in shaping MHC polymorphism across large spatial scales, while the interplay between gene flow and selection was stronger towards the northern peripheries. The similarity of MHC alleles within subspecies relative to their neutral genetic differentiation suggests that adaptive divergence among subspecies can be maintained despite ongoing gene flow along subspecies boundaries. Neutral genetic diversity was low in small relative to large populations, but MHC diversity within individuals was high in small populations. Despite reduced neutral genetic variation, small and isolated populations harbour functional variation that likely contribute to the species evolutionary potential at the northern range. Our findings suggest that conservation approaches should focus on managing adaptive variation across the species range rather than protecting subspecies per se.


Jager, C. P.,M. R. Duvall, B. J. Swanson, C. A. Phillips, M. J. Dreslik, S. J. Baker, and R. B. King. 2016. Microsatellite and major histocompatibility complex variation in an endangered rattlesnake, the Eastern Massasauga Sistrurus catenatus. Ecology and Evolution DOI: 10.1002/ece3.2159

Abstract:
Genetic diversity is fundamental to maintaining the long-term viability of populations, yet reduced genetic variation is often associated with small, isolated populations. To examine the relationship between demography and genetic variation, variation at hypervariable loci (e.g., microsatellite DNA loci) is often measured. However, these loci are selectively neutral (or near neutral) and may not accurately reflect genomewide variation. Variation at functional trait loci, such as the major histocompatibility complex (MHC), can provide a better assessment of adaptive genetic variation in fragmented populations. We compared patterns of microsatellite and MHC variation across three Eastern Massasauga (Sistrurus catenatus) populations representing a gradient of demographic histories to assess the relative roles of natural selection and genetic drift. Using 454 deep amplicon sequencing, we identified 24 putatively functional MHC IIB exon 2 alleles belonging to a minimum of six loci. Analysis of synonymous and nonsynonymous substitution rates provided evidence of historical positive selection at the nucleotide level, and Tajima's D provided support for balancing selection in each population. As predicted, estimates of microsatellite allelic richness, observed, heterozygosity, and expected heterozygosity varied among populations in a pattern qualitatively consistent with demographic history and abundance. While MHC allelic richness at the population and individual levels revealed similar trends, MHC nucleotide diversity was unexpectedly high in the smallest population. Overall, these results suggest that genetic variation in the Eastern Massasauga populations in Illinois has been shaped by multiple evolutionary mechanisms. Thus, conservation efforts should consider both neutral and functional genetic variation when managing captive and wild Eastern Massasauga populations.


Stedman, A. l., C. P. Jager, E. T. Hileman, B. C. Jellen, C. A. Phillips, B. J. Swanson, and R. B. King. 2016. Multiple paternity in three wild populations of Eastern Massasauga Sistrurus catenatus. Herpetological Conservation and Biology 11: 160-167

Abstract:
Multiple paternity is widespread among animals. Within snakes, multiple paternity has been well-documented with the exception of the family Elapidae. However, variation in the frequency of multiple paternity among populations is poorly documented and warrants further investigation. Here, we provide evidence for multiple paternity in three wild populations of the Eastern Massasauga (Sistrurus catenatus). We documented multiple paternity in six of 12 Pennsylvania litters, five of 12 Michigan litters, and two of two Illinois litters. Female body size did not influence the likelihood of multiple paternity. However, an increase in female size correlated with increased litter size. Including this study, multiple paternity is now documented in 21 snake species belonging to 15 genera and four families. These results have implications for the captive management and conservation of this endangered rattlesnake. Specifically, captive breeding programs, such as the Eastern Massasauga Species Survival Plan (SSP®), might consider providing opportunities for multiple paternity.


Dresser, C. M., M. L. Kuhlmann, and B. J. Swanson. 2016. Variation in native crayfish agonistic response to the invasion of the Rusty Crayfish Oronectes rusticus (Girard,1852). Journal of Crustacean Biology 36:129-137.

Abstract:
The consequences of biological invasions warrant continued research on the mechanisms underlying the spread of exotic species, yet interspecific behavioral interactions are largely overlooked as a contributing factor or consequence of introductions of exotic species. Our study evaluates how native crayfish species, Cambarus bartonii (Fabricius, 1798) and Orconectes propinquus (Girard, 1852), respond behaviorally to the invasion of the rusty crayfish, Orconectes rusticus (Girard, 1852) in the Upper Susquehanna River Basin, NY, USA using experiments in a semi-natural setting. We found significant effects of species, sex, year, novelty to invasion, and abiotic environment on the proportion of time native crayfish species exhibited agonistic behavior toward invading rusty crayfish. Cambarus bartonii females were generally more aggressive than males, particularly in year two, but the opposite was true for O. propinquus as males were more aggressive than females. Behavioral variation in recipient crayfish communities is a potential mechanism influencing the spread of introduced crayfishes although future study is necessary to assess the relative extent of such influence. The mechanisms driving the spread of invasive species are clearly complex and interactive, but the development of effective management plans is limited by the completeness of our understanding, which thus far has been lacking a substantial ethological component.


Torstrom, S. M., K. Pangle, and B. J. Swanson. 2014. Shedding subspecies: The influence of genetics on reptile subspecies taxonomy. Molecular Phylogenetics and Evolution

Abstract:
The subspecies concept influences multiple aspects of biology and management. The 'molecular revolution' altered traditional methods (morphological traits) of subspecies classification by applying genetic analyses resulting in alternative or contradictory classifications. We evaluated recent reptile literature for bias in the recommendations regarding subspecies status when genetic data were included. Reviewing characteristics of the study, genetic variables, genetic distance values and noting the species concepts, we found that subspecies were more likely elevated to species when using genetic analysis. However, there was no predictive relationship between variables used and taxonomic recommendation. There was a significant difference between the median genetic distance values when researchers elevated or collapsed a subspecies. Our review found nine different concepts of species used when recommending taxonomic change, and studies incorporating multiple species concepts were more likely to recommend a taxonomic change. Since using genetic techniques significantly alter reptile taxonomy there is a need to establish a standard method to determine the species-subspecies boundary in order to effectively use the subspecies classification for research and conservation purposes.


Steinwald, M. C., B. J. Swanson, J. M. Doyle, and P. M. Waser. 2013. Female mobility and the mating system of the banner-tailed kangaroo rat (Dipodomys spectabilis). Journal of Mammalogy: 94: 1258 - 1265.

Abstract:
Like some species of pika (Ochotona) and tree squirrel (Tamiasciurus), the banner-tailed kangaroo rat (Dipodomys spectabilis) is a solitary, philopatric larder-hoarder that practices unisexual territoriality. Seeking to understand how this unusual combination of traits might influence the mating system, we used systematic trapping at mounds (burrows) and spool-and-line tracking to examine male and female visits to each other. Where genetic data exist, unisexual larder-hoarders such as D. spectabilis have been found to be polygynandrous. We asked whether the fact that females sometimes mate with more than 1 male is a passive side effect of imperfect mate defense by males, or whether females actively engage in behaviors that encourage multiple mating. During the nonbreeding season, adults of both sexes were rarely captured at mounds other than their own. In contrast, during the breeding season females as well as males were significantly more likely to be captured away from their home mounds, most often at mounds belonging to adults of the opposite sex. Spool- and-line tracking during the breeding season confirmed these results. Consistent with the expectation that they engage in competitive mate searching, adult males visited adult females' mounds significantly more than expected by chance and without regard to age, size, or relatedness. More surprisingly, adult females exhibited similar behavior, expanding their home ranges and disproportionately visiting the mounds of large adult males during the nights preceding estrus. Increased (and apparently directed) female mobility during the days preceding estrus may serve as a means of shaping the pool of competing mates and is worthy of more attention in this and other, ecologically similar species.


Martinez-Bakker M. E., S. K. Sell, B.J. Swanson, B. P. Kelly, D. A. Tallmon. 2013. Combined Genetic and Telemetry Data Reveal High Rates of Gene Flow, Migration, and Long-Distance Dispersal Potential in Arctic Ringed Seals (Pusa hispida). PLoS ONE 8(10): e77125. doi:10.1371/journal.pone.0077125

Abstract:
Ringed seals (Pusa hispida) are broadly distributed in seasonally ice covered seas, and their survival and reproductive success is intricately linked to sea ice and snow. Climatic warming is diminishing Arctic snow and sea ice and threatens to endanger ringed seals in the foreseeable future. We investigated the population structure and connectedness within and among three subspecies: Arctic (P. hispida hispida), Baltic (P. hispida botnica), and Lake Saimaa (P. hispida saimensis) ringed seals to assess their capacity to respond to rapid environmental changes. We consider (a) the geographical scale of migration, (b) use of sea ice, and (c) the amount of gene flow between subspecies. Seasonal movements and use of sea ice were determined for 27 seals tracked via satellite telemetry. Additionally, population genetic analyses were conducted using 354 seals representative of each subspecies and 11 breeding sites. Genetic analyses included sequences from two mitochondrial regions and genotypes of 9 microsatellite loci. We found that ringed seals disperse on a pan-Arctic scale and both males and females may migrate long distances during the summer months when sea ice extent is minimal. Gene flow among Arctic breeding sites and between the Arctic and the Baltic Sea subspecies was high; these two subspecies are interconnected as are breeding sites within the Arctic subspecies.


Sundaram, M., J. R. Willoughby, AND B. J. Swanson. 2013. Indirect evidence of prey-switching in minks: empirical evidence, theoretical modeling, and spatial drivers. Journal of Mammalogy 94 (5): TBD.

Abstract:
A spatial gradient in the interactions between American minks (Neovison vison) and muskrats (Ondatra zibethicus) occurs in the Hudson's Bay Company fur harvest returns of Canada. Evidence for strong dependence of minks on muskrats exists in northwestern Canada, whereas evidence for weaker interactions exists in central and eastern Canada. We tested the hypothesis that minks consume fewer muskrats and more alternative prey in some areas, using fur records from 56 Hudson's Bay posts. Both muskrats and small microtines were found to explain mink dynamics, with small microtines and other alternative prey gaining importance in the eastern portion of our study area. Mink fur returns exhibited a range of cycle lengths from 2.6 to 13 years encompassing typical small microtine periodicities of 3-5 years and typical muskrat periodicities of 8-13 years. A time lag of 0 years occurred between mink and muskrat harvest data frequently in the eastern portion of our study area, hypothesized to be a result of minks consuming alternative prey. To biologically verify small microtines as a potential prey source, we modeled mink and muskrat population dynamics assuming small microtines were an alternative prey by modifying the Turchin and Hanski (1997) model. Simulated mink and muskrat time series replicated observed periodicity and time-lag range, suggesting that minks can be generalist predators and consume alternative prey. Finally, we examined species richness and land cover as potential drivers of mink prey-switching, but were unable to find support for either hypothesis, suggesting that additional environmentalor competition-related interactions influence mink population dynamics.


Ray, J.W., R. B. King, M. R. Duvall, J. W. Robinson, C. P. Jaeger, M. J. Dreslik, B. J. Swanson, Diane Mulkerin. 2013. Genetic Analysis and Captive Breeding Program Design for the Eastern Massasauga Sistrurus catenatus catenatus. Journal of Fish and Wildlife Management 4: 104 - 113.

Abstract:
The eastern massasauga Sistrurus catenatus catenatus is a declining species for which a captive breeding program was established in 2006. To effectively manage wild and captive populations, an understanding of genetic diversity within the species is necessary. We analyzed mitochondrial DNA sequences of 186 individuals: 109 wild snakes from 34 U.S. and Canadian counties and districts, all 52 breeding program members (23 of known and 29 of unknown origin), 18 other captives of unknown origin, and 7 outgroup representatives of desert massasauga S. c. edwardsii, and western massasauga, S. c. tergeminus. Statistical parsimony, maximum likelihood, and maximum parsimony analyses all identified eastern massasaugas as divergent from western and desert massasaugas. We found 18 different haplotypes among eastern massasaugas, comprising three geographically and genetically differentiated NADH dehydrogenase II (ND2) subunits that potentially reflect post-Pleistocene range expansion from unglaciated into formerly glaciated regions. Snakes of unknown origin could all be assigned unambiguously to these ND2 subunits. To maintain natural genetic variation, preserve diversity in captive lineages, and allow future augmentation or reintroduction, the Association of Zoos and Aquariums is managing these three geographic ND2 subunits separately within the Eastern Massasauga Species Survival Plan breeding program.


Dresser, C. and B.J. Swanson. 2013. Preemptive legislation inhibits the anthropogenic spread of an aquatic invasive species, the rusty crayfish (Orconectes rusticus). Biological Invasions 15: 1049-1056

Abstract:
The enactment of legal policies is often recommended to prevent anthropogenic introductions of invasive species. In this paper, we evaluated the effectiveness of proactive state legislative policies in deterring colonization by rusty crayfish (Orconectes rusticus) and the expected spread into previously uninvaded states using network-based spatial analysis. We found that the presence of regulations was positively associated with the presence of rusty crayfish (p = 0.027), but often regulations were put into effect subsequent to the invasion. Regulations that did not explicitly prohibit transport, applied to specific drainages, or prohibited only rusty crayfish were not effective. However, preemptive legislation was effective in reducing the likelihood of invasion, if regulations prohibited the transport of all live crayfish species between water bodies, as only 1 state which passed such legislation prior to invasion by rusty crayfish was subsequently colonized (S = 12, p =0.031). Five states are likely to be invaded by rusty crayfish via range expansion across interstate drainages, and dispersal rates suggest that all of these states could be colonized within 10 years. While it is unlikely that regulations will prevent dispersal-based invasion across state lines through shared drainages, preemptive legislation can significantly reduce anthropogenic spread of aquatic invasive species between drainages and effectively retard the expansion of rusty crayfish. Our results suggest that the most effective form of legislation is one that does not require individuals to identify species, thus we recommend states enact policies that explicitly prohibit the transport of all live crayfish between water bodies.


Willoughby, J. R., M. Sundaram, T. L. Lewis, and B.J. Swanson. 2013. Population decline in a long-lived species: The Wood Turtle in Michigan. Herpetologoca 69: 186 - 198.

Abstract:
Populations of Wood Turtles, Glyptemys insculpta, have steadily decreased over the past 30 yr because The eastern massasauga Sistrurus catenatus catenatusis a declining species for which a captive breeding program was established in 2006. To effectively manage wild and captive populations, an understanding of genetic diversity within the species is necessary. We analyzed mitochondrial DNA sequences of 186 individuals: 109 wild snakes from 34 U.S. and Canadian counties and districts, all 52 breeding program members (23 of known and 29 of unknown origin), 18 other captives of unknown origin, and 7 outgroup representatives of desert massasauga S. c. edwardsii, and western massasauga, S. c. tergeminus. Statistical parsimony, maximum likelihood, and maximum parsimony analyses all identified eastern massasaugas as divergent from western and desert massasaugas. We found 18 different haplotypes among eastern massasaugas, comprising three geographically and genetically differentiated NADH dehydrogenase II (ND2) subunits that potentially reflect post-Pleistocene range expansion from unglaciated into formerly glaciated regions. Snakes of unknown origin could all be assigned unambiguously to these ND2 subunits. To maintain natural genetic variation, preserve diversity in captive lineages, and allow future augmentation or reintroduction, the Association of Zoos and Aquariums is managing these three geographic ND2 subunits separately within the Eastern Massasauga Species Survival Plan breeding program.


Kierepka, E. M., E.K. Latch, and B.J. Swanson. 2012. Influence of sampling scheme on the inference of sex-biased gene flow in the American badger (Taxidea taxus). Canadian Journal of Zoology 90: 1231-1242.

Abstract:
Population genetics has fueled a substantial growth in studies of dispersal, a life-history trait that has important applications in ecology and evolution. Mammals typically exhibit male-biased gene f low, so this pattern often serves as a null hypothesis in empirical studies. Estimation of dispersal using population genetics is not without biases, so we utilized a combination of population genetic methods and simulations to evaluate gene f low within the American badger (Taxidea taxus (Schreber, 1777)), a highly elusive and poorly understood mustelid. A total of 132 badgers captured between 2001 and 2002 were genotyped at nine microsatellite loci to investigate fine-scale genetic structure consistent with philopatry in females and dispersal in males. Resultant genetic patterns were largely consistent with a panmictic population with little evidence for sex-biased dispersal, and simulations confirmed that our sampling scheme did not substantially impact our statistics. An overall deficiency of heterozygotes was observed across the Lower Peninsula, which indicates either a Wahlund effect, mixing of separate populations, or inbreeding. Our study emphasizes the importance in deciphering between actual behavioral mechanisms and sampling effects when interpreting genetic data to understand other factors that inf luence dispersal like population density and territoriality.


Ethier, D. M., A. Lafleche, B. J. Swanson, J. J. Nocera, and C. J. Kyle. 2012. Population subdivision and peripheral isolation in American badgers (Taxidea taxus) and implications for conservation planning in Canada. Canadian Journal of Zoology 90:630-639.

Abstract:
In Canada, three subspecies of American badgers (Taxidea taxus (Schreber, 1777)) traditionally are identified; two of which are listed as endangered because of their restricted geographic range and low population sizes. To verify their subspecific designations and genetic insularity, we analyzed mitochondrial control region sequences within and among badger subspecies (Taxidea taxus jacksoni Schantz, 1946, Taxidea taxus jeffersonii (Harlan, 1825), and Taxidea taxus taxus (Schreber, 1777)) from nine locations in Canada and bordering United States. Although subspecies designations were sup- ported (a priori subspecific designations, n = 3, AMOVA: FST = 0.40, p < 0.001), insular populations also were found within subspecific ranges as shown by spatial analysis of molecular variation, which suggested that our sample set consisted of five genetic groups (FST = 0.39, p < 0.001). These five distinct groupings included the subdivision of T. t. jef fersonii on either side of the Selkirk Mountains, and of T. t. jacksoni in the western part of its range grouping more closely with T. t. taxus of Manitoba. These results indicate that endangered populations of badgers may be more segregated than previously identified using morphological characteristics as proxies for subspecific designation. These results have important implications for the conservation of badgers in Canada, particularly of the two endangered subspecies.


Cain, C. M., T. M. Livieri, and B. J. Swanson. 2011. Genetic evaluation of a reintroduced population of black-footed ferrets (Mustela nigripes). Journal of Mammalogy 92:751-759.

Abstract:
The black-footed ferret (Mustela nigripes) went extinct in the wild when the last 18 known ferrets were captured for a captive-breeding program. Following the success of the captive-breeding program, 146 genetically nonessential ferrets were released at the Conata Basin, South Dakota, from 1996 to 1999. We conducted a genetic analysis of the Conata Basin black-footed ferret population from 2001 to 2003 to determine if genetic variation had been lost since the cessation of reintroductions and if demographic- and genetic-based estimates of effective population size (Ne) accurately predicted observed levels of heterozygosity. We used DNA from wild- born kits (n 5 254) in the Conata Basin population (2001-2003) to calculate current genetic diversity levels. Both allelic diversity (A 5 2, both subpopulations) and mean heterozygosity were low for both subpopulations -0.39 6 0.12 SE in Agate-Sage Creek and 0.39 6 0.16 SE in Heck Table, but not significantly different from estimates made in 1999. We found no significant difference between observed and expected heterozygosity levels. Demographic-based estimates of Ne were an order of magnitude higher than genetic-based estimates of Ne, but the 2 estimates provide a range of Ne values for the population. This study shows that the Conata Basin ferret population is able to maintain its genetic diversity over time despite its population history.


O'Neil, E., and B. J. Swanson. 2010. Using track-plate footprints in fisher mark-recapture population estimation. American Midland Naturalist 164: 165-171.

Abstract:
Obtaining accurate estimates of fisher (Martes pennanti) population abundance is challenging to resource management agencies given the large home ranges and low densities at which fisher occur. Current methods for estimating population abundance are expensive in terms of equipment required and hours worked indicating a need for a less labor and equipment intensive method. Track-plate footprinting is a method of individually identifying fisher by the papillae patterns found on the metacarpal pad. We evaluated the technique of track-plate footprinting as a mark-recapture method to estimate population abundance of fisher in the Ottawa National Forest of Michigan's Upper Peninsula. We placed covered track-plates using copy toner and a medium of contact paper as a method of obtaining footprints of fisher for individual identification. Over 1548 trap-nights we identified 24 prints from nine different fisher with four individuals being recaptured. Program Mark produced a population estimate of 13 animals with a 95% confidence interval of 8 to 20 animals. Our study shows that track-plate footprinting is a viable method for estimating population abundance of fisher under natural conditions.


Marsack, K., and B. J. Swanson. 2009. A genetic analysis of the impact of generation time and road-based habitat fragmentation on Eastern Box Turtles (Terrapene c. carolina). Copeia 2009: 647-652.

Abstract:
Historically, the Eastern Box Turtle (Terrapene c. carolina) was found in 31 counties in Michigan's Lower Peninsula, although it has been extirpated from 13 of those counties in the last ten years. One possible cause of the decline is road- based habitat fragmentation with resulting demographic and genetic consequences. Accurately identifying population structure is necessary to determine conservation units and aid in the recovery of Terrapene c. carolina. We genotyped 163 turtles at eight microsatellite loci from three locations in southwestern Michigan covering 360 km2. We found high levels of genetic variation (H = 0.83; A = 16) and low levels of genetic differentiation (FST = 0.006) in the system. The three areas exist as a single population and there was a low rate (11%) of misassignment across the sites. There was initial evidence of a genetic bottleneck in two of the three populations and the system as a whole. However, additional analysis failed to find a mode-shift in allele frequencies and did not detect any further evidence of a bottleneck in any of the populations. We conclude that the conflicting genetic indication of a bottleneck, despite the geographic evidence, is due to the long generation time of Terrapene c. carolina. Further, our study suggests that the retention of genetic variation despite population declines allows managers flexibility in dealing with the conservation of long-lived species.


Gregory, A. J., M. A. Lung, T. M. Gehring, and B. J. Swanson. 2009. The Importance of Sex and Spatial Scale When Evaluating Sexual Segregation by Elk in Yellowston. Journal of Mammalogy 90: 971-979.

Abstract:
The forage-selection hypothesis (FSH) explains sexual segregation in ungulates as a function of different dietary requirements producing different levels of habitat optimality, whereas the reproductive-strategy hypothesis (RSH) explains sexual segregation as a function of different survival strategies between the sexes. Based on observations of habitat use by elk (Cervus elaphus) in Yellowstone National Park, Wyoming with regard to varying levels of wolf encounter risk, we found that our determination of whether the RSH or FSH best applied to sexual segregation varied by the scale at which we were measuring habitat use. At broad spatial scales we found no significant avoidance of wolves by elk. At the habitat scale we found that habitat use by elk was consistent with predictions of the reproductive strategy in that female elk used habitats that offered a balance of forage and escape terrain for themselves and calves, and that the degree to which escape terrain was present was dependent upon the risk of wolf encounter. At the scale of the habitat patch we found that differences in forage availability likely drove the differences in habitat use. Our results highlight the importance of scale when investigating habitat use, nonlethal predation effects, and sexual segregation in ungulates.


Swanson, B. J. and C. J. Kyle 2007. Relative Influence of Temporal and Geographic Separation of Source Populations in a Successful Marten Reintroduction. Journal of Mammalogy 88: 1346-1348.

Abstract:
Reintroduced populations face a genetic bottleneck due to the founding event of the reintroduction. Bringing in additional animals from different locations, or at different times, can restore genetic variation to a reintroduced population and offset the founder event. The reintroduced population of martens in Michigan came from 3 different locations in Ontario and occurred over a 24-year period. The high level of genetic variation found in Michigan's reintroduced marten population could be due to the multiple source locations or the temporal separation of the reintroductions. Based on the genetic variation found in martens, the 3 source locations more likely represent subsamples from a single population and the observed level of genetic variation is due to the temporal separation of the reintroduction events.


Millions, D. G. and B. J. Swanson. 2007. Impact of Natural and Artificial Barriers to Dispersal on the Population Structure of Bobcats. Journal of Wildlife Management 71: 96-102.

Abstract:
We investigated population structure and genetic diversity for bobcats (Lynx rufus) in Michigan, USA, which are distributed throughout the upper peninsula (UP) and the northern half of the lower peninsula (LP) of Michigan. Specifically, we assessed the influence of natural and artificial barriers to dispersal on the genetic population structure of the bobcat across Michigan, as well as in each peninsula. We used 5 microsatellite markers and the statistical package STRUCTURE to identify populations and assign individuals to their population of origin. STRUCTURE identified one population in each peninsula, indicating that the UP and LP are genetically isolated by the Straits of Mackinac which divide the UP and LP. Despite a greater density of roads in the LP, we found no evidence that they have led to intrapeninsular population structure. Our results suggest that, from a genetic standpoint, management agencies do not need to be concerned about the fragmenting effects of roads when producing management plans for bobcat


Swanson, B. J., B. P. Kelly, C. K. Maddox and J. R. Moran. 2006. Shed Skin as a Source of DNA for Genotyping Seals. Molecular Ecology 6: 1006 - 1009.

Abstract:
Obtaining a sufficient number of DNA samples from ice-breeding marine phocids, in a noninvasive manner, has proven difficult and has limited the ability to use molecular genetics on these species. We evaluate the ability to genotype ringed seals using a novel source of DNA, skin cells shed by the seal as it moults on sea ice. We found that shed skin samples yielded a lower quantity and purity of DNA compared to tissue samples. Nevertheless, the shed skin cells were a viable source of DNA for microsatellite analysis; we found no significant difference in allelic diversity or heterozygosities between tissue samples and shed skin cells. This source of DNA should allow the rapid collection of a large number of noninvasively collected DNA samples in ice-breeding phocids.


Swanson, B. J., L. R. Peters, and C. J. Kyle. 2006. Demographic and Genetic Evaluation of an American Marten Reintroduction. Journal of Mammalogy 87: 272 - 280.

Abstract:
Reintroduced populations are generally smaller and more isolated than native populations; thus even when reintroduced populations are demographically stable, a lack of genetic variation may present a threat to long-term persistence. We examined the demographic structure and genetic variation of the marten reintroduction into the Upper Peninsula of Michigan. Male : female and juvenile : adult female ratios indicate that the Michigan population is demographically stable. Michigan martens had higher allelic diversity (A = 7.4) compared to the average diversity found among Canadian populations (A = 5.8) and similar levels of observed heterozygosity (HCanadian= 0.64, HMichigan= 0.63), excluding Newfoundland martens. We found no significant differences in the allelic diversity or heterozygosity between the reintroduced Michigan population and the source population for the reintroduction, that of Chapleau, Ontario. Surprisingly, we found no evidence of a genetic bottleneck in the Michigan population. We suggest that the genetic success of this reintroduction is a result of the multiple reintroductions and subsequent intrastate translocations that mimicked gene flow. The success was further aided by the presence of small remnant populations that remained in Michigan, as evidenced by the presence of private alleles in Michigan.


Swanson, B. J., and P. J. Rusz. 2006. Detection and Classification of Cougars in Michigan Using Low Copy DNA Sources. American Midland Naturalist 155: 363 - 372.

Abstract:
Sporadic reports of cougars (Puma concolor) have occurred in Michigan since its official classification as extirpated in the 1930s. We collected 297 scats from 12 areas in Michigan with heavy sighting reports of cougars. Ten scats produced DNA profiles consistent with cougars. One scat was identified as having a North American origin; the other nine scats produced no useable sequences. One pre-Columbian sample, from a Native American burial site; also matched the current North American genotype. Based on the distance between cougar scats, we conclude that there were at least eight cougars in Michigan during the 3 y of this study. The mtDNA sequences also suggest that at least some of the matrilines currently and historically found in Michigan are the same as those found in current and historical western populations.


Millions, D. G., and B. J.Swanson. 2006. An Application of Manel's Model: Detectig Bobcat Poaching in Michigan. The Wildlife Society Bulletin 34: 150 - 155.

Abstract:
The illegal harvest of natural resources (i.e., poaching) has the potential to threaten the persistence of many plant and animal species. In Michigan bobcats ( Lynx rufus) are distributed throughout the Upper Peninsula (UP) and the northern half of the Lower Peninsula (LP) and are a biologically and economically important species. The popularity of bobcat hunting and trapping in Michigan, along with different harvest regulations between the 2 peninsulas, has created the need for a reliable method of identifying incidences of poaching. Because the bag limit is higher in the UP, we hypothesized that some bobcats harvested in the LP are being registered as originating from the UP. We used 8 polymorphic microsatellite markers and the statistical package STRUCTURE to assign individuals to the population in which they had the highest likelihood of occurrence based on their genotype. We evaluated the influence of using posterior probability threshold values from T . 0.9 - 0.999 on the number of animals classified as poached. Based on this range, STRUCTURE produced correct assignment rates of 53 - 82%. All instances of genetic re-assignment involved bobcats claimed as harvested in the UP but genetically assigned to the LP following the suspected method of bobcat poaching in Michigan. This approach provides a reliable method of determining the source population for bobcats harvested in the state and should provide enforcement agencies with a useful way of identifying potential poaching cases.


Steinwald, M. C., B. J. Swanson, and P. M. Waser. 2006. Effects of spool-and-line tracking on small desert mammals. Southwestern Naturalist 51: 71 - 78.

Abstract:
Spool-and-line tracking is an innovative and inexpensive way to record the movements of small mammals in a variety of habitats, and could have important applications for conservation related studies. However, the potential negative effects of the method have not been investigated. We document the effects of spool-and-line tracking on short-term change in body mass, recapture, and survival probability of banner-tailed kangaroo rats, Dipodomys spectabilis, in southeastern Arizona. We attached spools to D. spectabilis adults of both sexes during 3 years of varying environmental conditions, with total sample sizes of 90 experimental and 81 control animals. We did not attach spools to females in late pregnancy, and, to avoid entanglement, we did not attach spools to kangaroo rats located within 25 m of each other on the same night. We found no significant negative effects of spool attachment on body mass, survival, or recapture probability in either sex in any year.


Swanson, B. J., R. T. Fuhrman, R. L. Crabtree. 2005. Elevational isolation of red fox populations in the Greater Yellowstone ecosystem. Conservation Genetics 6:123-131.

Abstract:
Foxes in the Greater Yellowstone Ecosystem are reported to show high frequencies of blonde and gray coat 12 colors. A survey of park sighting records showed that the frequency of the novel coat colors significantly increases at elevations greater than 2300 m, suggesting some form of elevational isolation. We evaluated the degree of genetic separation between the high-elevation foxes (>2300 m) and contiguous populations of foxes at mid-elevations (1600 - 2300 m). Low-elevation (<1600 m) foxes from North Dakota, >1000 km straight line distance from our populations, were used as a control group. We genotyped 15 high-elevation, 15 mid-elevation, and 10 low-elevation foxes at 10 microsatellite loci each. Heterozygosity was significantly lower in both the high-elevation and mid-elevation populations compared to the low-elevation foxes. The genetic differentiation was significantly greater between the high-elevation and mid-elevation foxes than between the mid-elevation and low-elevation foxes. Similarly, estimates of RST and FST suggest less gene flow occurs between the contiguous high- and mid-elevation fox populations than between the mid- and low-elevation fox populations separated by >1000 km. The assignment test further supports this hypothesis. Although further work is needed, we suggest that the high-elevation foxes are remnant populations from the Wisconsin glaciation and should be managed as a unique population.


Davis, C., Keane, B., Swanson, B., Loew, S., Waser, P. M., Strobeck, C., and Fleischer, R. C. 2000. Characterization of microsatellite loci in bannertailed and giant kangaroo rats, Dipodomys spectabilis and Dipodomys ingens.

Development of microsatellite primers for kangaroo rats.


Johnson, D.R., Swanson, B. J., and Eger, J. L. 2000. Cyclic dynamics of eastern Canadian ermine populations. Canadian Journal of Zoology 78: 835 - 839.

Abstract:
Based on partial autocorrelation analysis, 20 ermine ( Mustela erminea) populations in Manitoba, Ontario, and Quebec demonstrated cyclic dynamics characterized by a latitudinal gradient of decreasing first-order feedback and increasing negativity of second-order feedback. Most of these population exhibited three cyclic peaks and a 10-year interval of noncyclic dynamics during the sampling period (1915-1940). Changes in ermine density probably reflected those in the density of microtine rodents, their primary prey. Analysis of the limited number of long-term lemming and vole series from boreal North America indicated a latitudinal gradient in cyclic dynamics similar to that of microtine rodent populations in northern Eurpoe. Complex geographical and temporal variation in ermine population dynamics, including cyclic, noncyclic, and shifting patterns of density change, supports the specialist-generalist hypothesis of predator-prey interaction at temperate latitudes.


Swanson, B. J., and Johnson, D. R. 1999. Distinguishing causes of intraspecific synchrony in population dynamics. Oikos 86: 265 - 274.

Abstract:
We examined the degree and cause of intraspecific synchrony in population dynamics between 29 - 42 populations for each of seven mammalian species. Regions containing multiple populations with similar dynamics were identified using cluster ananlysis. Two explanations for the observed syncrhony were evaluated, dispersal and the "Moran effect", a spatially correlated density independent perturbation, such as weather, which occurs across populations. Populations synchronized by dispersal are expected to exhibit a negative relationship between synchrony and distance, while populations synchronized by a Moran effect must have a similar density dependent structure (DDS). To distinguish between these hypotheses we used autoregressive modeling to determine the DDS of each pouplation, and cross-correlation to estimate the degree of synchrony between two populations. Dispersal alone was assumed to be responsible for synchrony in populations with a significant negative synchrony-distance (S-D) relationship and heterogeneous DDS. We assumed that a Moran effect could have produced synchrony in populations with homogeneous DDS and a non-significant S-D relationship. It was not possible to assign synchrony to a single factor in regions with a homogeneous DDS and a significant S-D relationship, and we excluded the possibility of a Moran effect in regions with heterogenous DDS and a non-significant S-D relationship. Using these criteria, we identified dispersal as synchronizing populations withing one region each of ermine, lynx, mink, and red fox and in two regions of muskrat. A Moran effect may have synchronized one region of ermine, fisher, lynx, and mink, although we were unable to identify a causative factor. One lynx region and one mink region showed characteristics of both dispersal and Moran-based synchrony, and 9 regions of synchrony could not be assigned to either factor. These results show that by examining the DDS and S-D relationship we were able to determine the factors most likely responsible for synchronzied population dynamics in 10 of 21 cases. Possible cases of Moran-based synchrony do not appear to be common, occurring in only 18.2% of these regions. It should also be noted that just as correlation does not imply causation, presence of homogeneous DDS does not indicate a Moran effect, only its possible occurrence.


Swanson, B. J. 1998. Autocorrelated rates of change in animal populations and their relationship to precipitation. Conservation Biology 12: 801-808.

Abstract:
I examined the prevalence of autocorrelation was in mammalian, avian, and precipitation time series, how well autocorrelation in the environment translates into autocorrelation in animal populations, and length of time series needed to accurately characterize the degree of autocorrelation. These are important questions, as more complex population models incorporate autocorrelation terms in life history characteristics and the intrinsic rate of increase. Including inaccurate or nonsignificant autocorrelation can alter the conclusions reached, providing either an unduly rosy or bleak picture of the likelihood of population viability and persistence. Using autocorrelation analysis in 175 vertebrate and 88 precipitation data sets, I found that 17.8% of the mammalian time series, 61.5% of the avian time series, and 97.8% of the precipitation data sets were autocorrelated. Carnivore populations were more likely to show significant autocorrelation at lags of 2 or more years than herbivore populations. I found only two cases of significant cross correlation between rate of population increase and local precipitation that were significant. This indicates that, although some environmental variables may be highly autocorrelated, it does not translate into autocorrelation in the resident animal populations. Based on subsampling of the precipitation and vertebrate data, I found 15 years of data is sufficient to produce an autocorrelation that is not significantly different from one based on 100 years of data, although the variance continues to decrease with the length of the time series as expected. My results suggest that while some populations show temporal autocorrelation, it is not ubiquitous, and environmental autocorrelation may not be a good predictor of autocorrelation in rates of increase. Population modelers should determine if autocorrelation exists in populations of interest prior to modeling their viability or probability of persistence as not all population are equally influenced by autocorrelation.

Swanson, B. J. and D. R. Johnson. 1996. Spatial and temporal trends and effects of population size on the frequency of color phenotypes in the wild red fox (Vulpes vulpes). Canadian Journal of Zoology 74: 1622-1631.

Abstract:
We analyzed the hypothesized relationships of temporal, spatial, and harvest trends with frequency of red fox (Vulpes vulpes) color morphs in 57 Hudson's Bay Company posts over a 20- to 26-year period, but found none of the strong relationships postulated to exist. A meta-analysis of each data set suggested a weak inverse relationship between latitude and frequency of the red morph. Meta-analysis further indicated a weak positive relationship with time and the frequency of the red phase, although this trend was not due to climate change. No relationship was found between harvest size and color phase, or between a 1-year lagged harvest size and color phase, which evaluated the effects of dispersal. The data sets did not allow conclusive determination of the mechanisms behind the trends, but it is postulated that a slight selective advantage is found for the dark morphs at high latitudes, while the temporal increase in frequency of the red phenotype is probably the result of northward dispersal from southern populations.

 

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