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Relatedness and other finescale population genetic analyses in the threatened eastern box turtle (Terrapene c. carolina) suggest unexpectedly high vagility with important conservation implications

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Abstract

Genetic analyses of populations are essential to the conservation of threatened and cryptic taxa such as Chelonians. Turtles and tortoises are among the most imperiled vertebrate taxa worldwide, yet many of the natural history traits remain unknown leaving management decisions ill- or improperly informed. The eastern box turtle Terrapene c. carolina is no exception, with many gaps in our knowledge about traits such as juvenile dispersal and patterns of relatedness across the landscape, especially as it is a species not particularly tied to water and vulnerable to human disturbance. In addition, all long-term studies of this species have documented demographic population declines, even in protected habitats. In this study we explore finescale population structuring, gene flow, dispersal, and relatedness at four sites across the species range. These sites vary in habitat fragmentation and surrounding habitat quality. Many radiotelemtery and mark-recapture studies suggest that Terrapene spp. have a sedentary natural history, with small and temporally conserved home ranges and little propensity for dispersal. Based on these data we predicted that populations would be highly structured at fine geographic scales, closely related individuals (1st- and 2nd-degree relatives) would coexist in close proximity, and individuals exhibiting transient behavior would be true transients. All sites had low levels of population structuring, mean pairwise relatedness values were statistically zero, over 90 % of pairs of individuals were unrelated, 4.4–8.7 % were half-siblings, and fewer than 1.0 % were full siblings or parent-offspring pairs. These patterns were consistent across all four sites, regardless of habitat fragmentation. Furthermore, while some related pairs were found within a few meters of each other, others ranged up to 33 km apart. We found that one of two individuals with transient behavior was indeed a true genetic transient. These findings suggest that box turtles may be much more vagile than current management practices recognize. As most turtle species are strongly affected by anthropogenic disturbance, many may require much larger contiguous blocks of intact habitat for species persistence as the box turtle likely does. Management plans may therefore need to be updated to allow for safe and effective long-distance dispersal at the appropriate spatial scales in order to maintain genetic health of these species.

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Acknowledgments

We thank samplers including M. Allender, M. Baragona, K. Buhlmann, V. Clarkston, K. Creely, M. Cook, M. Cross, N. Engbrecht, E. Estabrook, J. Faller, S. Foertmeyer, A. Garcia, B. Geboy, S. Hagood, K. Hanauer, P. Henry, A. Hoffman, L. Jedele, B. Johnson, S. Johnson, N. Karraker, L. Keener-Eck, V. Kinney, J. Kissel, S. Klueh, A. Krainyk, K. Lilly, J. MacNeil, J. Mitchell, T. Mitchell, K. Norris, H. Powell, K. Powers, J. Richards, J. Riegel, S. Ritchie, J. Shuey, G. Stephens, B. Tomson, T. Tuberville, M. Turnquist, B. Weigel, K. Westerman, M. Wildnauer, and L. Woody. We thank all members of the Williams lab for improving the manuscript. R. Burke, G. Dharmarajan, K. Dodd, J. Fike, R. Howard, G. Nyberg, S. Klueh, M. Kremer, M. Lannoo, N. Lichti, Z. Olson, K. Smith, B. Pauli, and E. Latch also gave important support. Support provided by the Indiana Department of Natural Resources, Division of Fish and Wildlife, Wildlife Diversity Section, State Wildlife Improvement Grant E2-08-WDS15; Indiana Division of Forestry Grant E-9-6-A558; and the Department of Forestry and Natural Resources, Purdue University. Research was conducted under the Purdue University Animal Care and Use Protocol 07-037 and amendments thereto.

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Kimble, S.J.A., Rhodes, O.E. & Williams, R.N. Relatedness and other finescale population genetic analyses in the threatened eastern box turtle (Terrapene c. carolina) suggest unexpectedly high vagility with important conservation implications. Conserv Genet 15, 967–979 (2014). https://doi.org/10.1007/s10592-014-0592-1

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