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Conservation genetics of the alligator snapping turtle: cytonuclear evidence of range-wide bottleneck effects and unusually pronounced geographic structure

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Abstract

A previous mtDNA study indicated that female-mediated gene flow was extremely rare among alligator snapping turtle populations in different drainages of the Gulf of Mexico. In this study, we used variation at seven microsatellite DNA loci to assess the possibility of male-mediated gene flow, we augmented the mtDNA survey with additional sampling of the large Mississippi River System, and we evaluated the hypothesis that the consistently low within-population mtDNA diversity reflects past population bottlenecks. The results show that dispersal between drainages of the Gulf of Mexico is rare (F STmsat  = 0.43, ΦSTmtDNA = 0.98). Past range-wide bottlenecks are indicated by several genetic signals, including low diversity for microsatellites (1.1–3.9 alleles/locus; H e = 0.06–0.53) and mtDNA (h = 0.00 for most drainages; π = 0.000–0.001). Microsatellite data reinforce the conclusion from mtDNA that the Suwannee River population might eventually be recognized as a distinct taxonomic unit. It was the only population showing fixation or near fixation for otherwise rare microsatellite alleles. Six evolutionarily significant units are recommended on the basis of reciprocal mtDNA monophyly and high levels of microsatellite DNA divergence.

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Acknowledgments

We thank B. W. Bowen for valuable comments on an early draft of the manuscript, M. Crepeau for preparing and shipping DNA aliquots, N. Lang for laboratory assistance, F. Janzen for helpful advice, C.-H. Kuo for providing his data on ornate box turtle, and personnel of the Sequoyah, Tishomingo, and Little River national wildlife refuges for their cooperation. We extend deep gratitude to the many individuals that helped with collecting alligator snapping turtles or gaining access to museum specimens, most recently, S. Baker, R. Brandon, M. Dreslik, R. Gillespie, J. Hartleb, S. Krueger, D. Ligon, J. MacGregor, M. Mahoney, D. Moore, A. Resetar, L. Rodman, A. Scott, L. Willis, and E. Zimmerer. Financial support provided by State Wildlife Grants under Project T-5-P of the Oklahoma Department of Wildlife Conservation and administered through the Oklahoma Cooperative Fish and Wildlife Research Unit (cooperators are Oklahoma State University, Oklahoma Department of Wildlife Conservation, United States Geological Survey, United States Fish and Wildlife Service, and Wildlife Management Institute). Financial support was also provided by the US Fish and Wildlife Service, the Division of Natural Heritage of the Illinois Department of Natural Resources and the Department of Zoology, Oklahoma State University. The use of trade, product, industry or firm names or products or software or models, whether commercially available or not, does not constitute endorsement by the US Government or the US Geological Survey.

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Authors and Affiliations

  1. Department of Zoology, Oklahoma State University, Stillwater, OK, 74078, USA

    A. A. Echelle, J. C. Hackler, J. B. Lack, S. F. Fox & R. A. Van Den Bussche

  2. Illinois Department of Natural Resources, Division of Natural Heritage, 9053 Route 148, Marion, IL, USA

    S. R. Ballard

  3. Gund Institute for Ecological Economics, University of Vermont, Burlington, VT, USA

    J. Roman

  4. Oklahoma Cooperative Fish and Wildlife Research Unit, US Geological Survey, Oklahoma State University, Stillwater, OK, USA

    D. M. Leslie Jr.

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  1. A. A. Echelle
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  2. J. C. Hackler
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  7. D. M. Leslie Jr.
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  8. R. A. Van Den Bussche
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Correspondence to A. A. Echelle.

Appendix 1

Appendix 1

Specimens assayed. Locality number and drainage name in bold (Fig. 1). Number of turtles assayed in parentheses (mtDNA/microsatellites). Museum sources are listed under the following acronyms: FMNH = Field Museum of Natural History, Chicago, ISM = Illinois State Museum, Springfield, UIMNH = University of Illinois Museum of Natural History, APU = Austin Peay State University, Tennessee.

1 Trinity River (3/3); Bedias Creek, Madison and Leon Counties, Texas (3/3). 2 Neches River (18/11); Bingham Lake, Tyler County, Texas (18/11). 3A Middle Mississippi River (13/13); Wolf Bayou Conservation Area, Pemiscott County, Missouri (7/7), FMNH 3234, Ohio River at Cairo, Alexander County, Illinois (1/1), UIMNH 33124, Mississippi River at Chester, Randolph County, Illinois (1/1), Wolf Creek, Jackson County, Illinois (1/1), ISM 689915, Dutch Creek, Union County, Illinois (1/1), APU #0-10,11, Kentucky Lake at Whiteoak Creek, Houston County, Tennessee (1/1), APU #1-3, Kentucky Lake at Tischel Bay, Stewart County, Tennessee (1/1). 3B White River (12/12); Black River, Butler County, Missouri (11/11), Cache River, unknown county, Arkansas (1/1). 3C Arkansas River (33/33); Little Vian Creek, Sequoyah County, Oklahoma (8/8), Big Vian Creek, Sequoyah County, Oklahoma (8/8), Hezekiah Creek, Sequoyah County, Oklahoma (4/4), Dirty Creek, Muskogee County, Oklahoma (12/12), Briar Creek, Haskell County, Oklahoma (1/1). 3D Canadian River (10/10); Mill Creek, McIntosh County, Oklahoma (10). 3E Little and Kiamichi rivers (6/6); Hugo Lake, Choctaw County, Oklahoma (1/1), Mill Creek, Pushmataha County, Oklahoma (1/1), Mud Creek, McCurtain County, Oklahoma (1/1) Forked Lake, McCurtain County, Oklahoma (3/3). 3F Lower Red River (4/4); Coushatta Bayou, Red River Parish, Louisiana (4/4), 3G Lower Mississippi River (13/6); Tensas River, Madison Parish, Louisiana (1/1), Bayou Gallion, Morehouse Parish, Louisiana (3/2,) Bayou Desiard, Ouachita Parish, Louisiana (5/2), Bayou D’Arbonne, Union Parish, Louisiana (1/1). 4 Pascagoula River (13/13); Pascagoula River, Jackson County, Mississippi (13/3). 5 Mobile Bay (12); Bear Creek, Baldwin County, Alabama (3/3), Southern Delta, Balwin County, Alabama, (2/2) Turkey Creek, Baldwin County, Alabama (5/5), Tallapoosa River, Macon County, Alabama (1/1), Lost Creek, Walker County, Alabama (1/1). 6 Perdido Bay (1/1); Styx River, Baldwin County, Alabama (1/1). 7 Pensacola Bay (23/20); Conecuh River, Covington-Crenshaw counties, Alabama (4/4), Escambia River, Escambia County, Alabama (5/4), Escambia River, Santa Rosa County, Florida (1/1), East Bay River, Okaloosa County, Florida (4/3), Shoal River, Okaloosa County, Florida (3/3), Yellow River, Okaloosa County, Florida (4/3), Blackwater River, Santa Rosa County, Florida (2/2). 8 Choctawhatchee River (2/2); Holmes Creek, Washington County, Florida (2/2). 9 Econfina River (8/2); Blue Springs, Washington County, Florida (8/2). 10 Apalachicola River (25/23); Apalachicola River, Calhoun County, Florida (1/1), The Bayou, Calhoun County, Florida (15/15), Chipola River, Jackson County, Florida (9/7). 11 Ochlockonee River (10/10); Ochlockonee River, Liberty County, Florida (5/5), Ochlockonee River, Leon County, Florida (2/2), Ochlockonee River, Wakulla County, Florida (3/3). 12 Suwannee River (18/15); Withlacoochie River, Lowndes County, Georgia (1/0), Alapaha River, Lowndes County, Georgia (1/0), Santa Fe River, Alachua and Union counties, Florida (10/9), New River, Union County, Florida (1/1), Suwannee River, Dixie County, Florida (3/3), Suwannee River, Suwannee County, Florida (2/2).

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Echelle, A.A., Hackler, J.C., Lack, J.B. et al. Conservation genetics of the alligator snapping turtle: cytonuclear evidence of range-wide bottleneck effects and unusually pronounced geographic structure. Conserv Genet 11, 1375–1387 (2010). https://doi.org/10.1007/s10592-009-9966-1

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