Polyandry and multiple paternities in the threatened Agassiz's desert tortoise, Gopherus agassizii

Conservation Genetics

Volumn 12, Issue 5, 2011, Pages 1313-1322

  Davy, Christina M ^a   Edwards, Taylor ^b   Lathrop, Amy ^c   Bratton, Mark ^d   Hagan, Mark ^e   Henen, Brian ^f   Nagy, Kenneth A ^g   Stone, Jonathon ^h   Hillard, L Scott ^g   Murphy, Robert W ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ARIZONA   (United States)

^c DEPARTMENT OF NATURAL HISTORY   (Canada)

^d AIR FORCE RESEARCH LABORATORY   (United States)

^e USAF   (United States)

^f Natural Resources and Environmental Affairs   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h MCMASTER UNIVERSITY   (Canada)

Author keywords

CERVUS; Chelonids; Microsatellites; Reproductive strategy; Tortoise conservation

Indexed keywords

ALLELE; CLUTCH SIZE; CONSERVATION MANAGEMENT; DESERT; DETECTION METHOD; ENDANGERED SPECIES; GENETIC MARKER; GENOTYPE; PATERNITY; POLYANDRY; QUANTITATIVE ANALYSIS; RELATEDNESS; REPRODUCTIVE STRATEGY; SPECIES CONSERVATION; TURTLE;

CALIFORNIA; UNITED STATES;

GOPHERUS AGASSIZII;

EID: 80052488471     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-011-0232-y     Document Type: Article

References (63)

1. Bacher J, Hennes LF, Gu T, Tereba A, Micka KA, Sprecher CJ, Lins AM, Amiott EA, Rabbach DR, Taylor JA, Helms C, Donis-Keller H, Schumm JW (1999) Pentanucleotide repeats: highly polymorphic genetic markers displaying minimal stutter artifact. In: Proceedings from the ninth international symposium on human identification, Orlando, pp 24-37.
2. Berry K, Morafka D, Murphy RW (2002) Defining the desert tortoise(s): our first priority for a coherent conservation strategy. Chelonian Conserv Biol 4: 249-262.
3. Bollmer J, Irwin M, Rieder J, Parker P (1999) Multiple paternity in loggerhead turtle clutches. Copeia 1999: 475-478.
4. Crim J, Spotila L, Spotila J, O'Connor M, Reina R, Williams C, Paladino F (2002) The leatherback turtle, Dermochelys coriacea, exhibits both polyandry and polygyny. Mol Ecol 11: 2097-2106.
5. Curtis C, Williams C, Spotila J (2000) Mating system of Caribbean leatherback turtles as indicated by analysis of microsatellite DNA from hatchlings and adult females. In: Proc 18th annual symposium on sea turtle biology and conservation (Compilers: Abreu-Grobois FA, Briseño-Dueñas R, Márques R, Sarti L). NOAA Tech. Memo. US Department of Commerce-SEFC-241, p 155.
6. Dutton P, Bixby E, Davis S (2000) Tendency towards single paternity in leatherbacks detected with microsatellites. In: Proc 18th annual symposium on sea turtle biology and conservation (Compilers: Abreu-Grobois FA, Briseño-Dueñas R, Márques R, Sarti L). NOAA Tech. Memo. US Department of Commerce-SEFC-241, p 39.
7. Edwards T, Goldberg C, Kaplan M, Schwalbe C, Swann DE (2003) PCR primers for microsatellite loci in the desert tortoise (Gopherus agassizii, Testudinidae). Mol Ecol Notes 3: 589-591.
8. Edwards T, Schwalbe CR, Swann DE, Goldberg CS (2004) Implications of anthropogenic landscape change on inter-population movements of the desert tortoise (Gopherus agassizii). Conserv Genet 5: 485-499.
9. Edwards T, Lathrop A, Ngo A, Choffe K, Murphy RW (2010) STR/microsatellite primers for the desert tortoise, Gopherus agassizii, and its congeners. Conserv Genet Res 3: 365-368.
10. Engstrom T, Edwards T, Osentoski M, Myers E (2007) A compendium of PCR primers for mtDNA, microsatellite, and other nuclear loci for freshwater turtles and tortoises. In: Shafer HB, FitzSimmons NN, Georges A, Rhodin AGJ (eds) Defining turtle diversity: proceedings of a workshop on genetics, ethics, and taxonomy of freshwater turtles and tortoises. Chelonian Res Monographs No 4, pp 124-141.
11. Ernst C, Lovich J (2009) Turtles of the United States and Canada, 2nd edn. Johns Hopkins University Press, Baltimore.
12. Fantin C, Santos Viana L, Monjeló LAS, Pires Farias I (2008) Polyandry in Podocnemis unifilis (Pleurodira; Podocnemididae), the vulnerable yellow-spotted Amazon River turtle. Amphib Reptil 29: 479-486.
13. Fantin C, Farias IP, Monjeló LAS, Hrbek T (2010) Polyandry in the red-headed river turtle Podocnemis erythrocephala (Testudines, Podocnemididae) in the Brazilian Amazon. Genet Mol Res 9: 435-440.
14. FitzSimmons NN (1998) Single paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas). Mol Ecol 7: 575-584.
15. FitzSimmons NN, Moritz C, Moore SS (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol Biol Evol 12: 432-440.
16. Galbraith DA (1993) Multiple paternity and sperm storage in turtles. Herpetol J 3: 117-123.
17. Galbraith D, White B, Brooks R, Boag P (1993) Multiple paternity in clutches of snapping turtles (Chelydra serpentina) detected using DNA fingerprints. Can J Zool 71: 318-324.
18. Germano DJ (1992) Longevity and age-size relationships of populations of desert tortoises. Copeia 1992: 367-374.
19. Germano DA (1994) Growth and age at maturity of North American tortoises in relation to regional climates. Can J Zool 72: 918-931.
20. Goldberg CS, Kaplan ME, Schwalbe CR (2003) From the frog's mouth: buccal swabs for collection of DNA from amphibians. Herpetol Rev 34: 220-221.
21. Hagerty BE, Tracy CR (2010) Defining population structure for the Mojave desert tortoise. Conserv Genet 11: 1795-1807.
22. Hagerty BE, Nussear KE, Esque TC, Tracy CR (2011) Making molehills out of mountains: landscape genetics of the Mojave desert tortoise. Landscape Ecol 2: 267-280.
23. Harry JL, Briscoe DA (1988) Multiple paternity in the loggerhead turtle (Caretta caretta). J Hered 79: 96-99.
24. Hauswaldt JS, Glenn TC (2003) Microsatellite DNA loci from the diamondback terrapin (Malaclemys terrapin). Mol Ecol Notes 3: 174-176.
25. Hernandez-Divers SM, Hernandez-Divers SJ, Wyneken J (2002) Angiographic, anatomic and clinical technique descriptions of a subcarapacial venipuncture site for chelonians. J Herpetol Med Surg 12: 32-37.
26. Hoekert WEJ, Neufeglise H, Schouten AD, Menken SBJ (2002) Multiple paternity and female-biased mutation at a microsatellite locus in the olive ridley sea turtle (Lepidochelys olivacea). Heredity 89: 107-113.
27. Ireland JS, Broderick AC, Glen F, Godley BJ, Hays GC, Lee PLM, Skibinski DOF (2003) Multiple paternity assessed using microsatellite marker, in green turtles Chelonia mydas (Linnaeus, 1758) of Ascension Island, South Atlantic. J Exp Mar Biol Ecol 291: 149-160.
28. Jensen MP, Abreu-Grobois FA, Frydenberg J, Loeschcke V (2006) Microsatellites provide insight into contrasting mating patterns in arribada vs. non-arribada olive ridley sea turtle rookeries. Mol Ecol 15: 2567-2575.
29. Johnston EE, Rand MS, Zweifel SG (2006) Detection of multiple paternity and sperm storage in a captive colony of the central Asian tortoise, Testudo horsfieldii. Can J Zool 84: 520-526.
30. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16: 1099-1106.
31. Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17: 3973-3977.
32. Kichler K, Holder MT, Davis SK, Marquez MR, Owens DW (1999) Detection of multiple paternity in Kemp's ridley sea turtle with limited sampling. Mol Ecol 8: 819-830.
33. Lamb T, Avise JC, Gibbons JW (1989) Phylogeographic patterns in mitochondrial DNA of the desert tortoise (Xerobates agassizii), and evolutionary relationships among North American gopher tortoises. Evolution 43: 76-87.
34. Lee PLM, Hays GC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proc Natl Acad Sci USA 101: 6530-6535.
35. McCracken GF, Burghardt GM, Houts SE (1999) Microsatellite markers and multiple paternity in the garter snake Thamnophis sirtalis. Mol Ecol 8: 1475-1479.
36. McTaggart S (2000) Good genes or sexy sons? Testing the benefits of female mate choice in the painted turtle, Chrysemys picta. Dissertation, University of Guelph.
37. Moon JC, McCoy ED, Mushinsky HR, Karl SA (2006) Multiple paternity and breeding system in the gopher tortoise Gopherus polyphemus. J Hered 97: 150-157.
38. Moore MK, Ball RM (2002) Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis. Mol Ecol 11: 281-288.
39. Murphy RW, Berry KH, Edwards T, McLuckie AM (2007) A genetic assessment of the recovery units for the Mojave population of the desert tortoise, Gopherus agassizii. Chelonian Conserv Biol 6: 229-251.
40. Murphy RW, Berry KH, Edwards T, Leviton AE, Lathrop A, Riedle JD (2011) The dazed and confused identity of Agassiz's land tortoise, Gopherusagassizii (Testudines: Testudinidae) with the description of a new species, and its consequences for conservation. ZooKeys 113: 39-71.
41. Neff BD, Pitcher TE, Repka J (2002) A Bayesian model for assessing the frequency of multiple mating in nature. J Hered 93: 406-414.
42. Niblick HA, Rostal DC, Classen T (1994) Role of male-male interactions and female choice in the mating system of the desert tortoise, Gopherus agassizii. Herpetol Monogr 8: 124-132.
43. Palmer KS, Rostal DC, Grumbles JS, Mulvey M (1998) Long-term sperm storage in the desert tortoise (Gopherus agassizii). Copeia 1998: 702-705.
44. Peare T, Parker PG (1996) Local genetic structure within two rookeries of Chelonia mydas (the green turtle). Heredity 77: 619-628.
45. Pearse DE, Anderson EC (2009) Multiple paternity increases effective population size. Mol Ecol 18: 3124-3127.
46. Pearse DE, Janzen FJ, Avise JC (2001) Genetic markers substantiate long-term storage and utilization of sperm by female painted turtles. Heredity 86: 378-384.
47. Pearse DE, Janzen FJ, Avise JC (2002) Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav Ecol Sociobiol 51: 164-171.
48. Pearse DE, Dastrup RB, Hernandez O, Sites JW (2006) Paternity in an Orinoco population of endangered Arrau River turtles, Podocnemis expansa (Pleurodira; Podocnemididae), from Venezuela. Chelonian Conserv Biol 5: 232-238.
49. Refsnider JM (2009) High frequency of multiple paternity in Blanding's turtle (Emys blandingii). J Herpetol 43: 74-81.
50. Rieder J, Parker P, Spotila J, Irwin M (1998) The mating system of the leatherback turtle: a molecular approach. In: Proc 16th symposium on sea turtle biology and conservation (Compilers: Byles R, Fernandez Y). NOAA Tech. Memo. US Department of Commerce-SEFC-241, p 120.
51. Roques S, Díaz-Paniagua C, Andreu AC (2004) Microsatellite markers reveal multiple paternity and sperm storage in the Mediterranean spur-thighed tortoise, Testudo graeca. Can J Zool 82: 153-159.
52. Roques S, Díaz-Paniagua C, Portheault A, Pérez-Santigosa N, Hidalgo-Vila J (2006) Sperm storage and low incidence of multiple paternity in the European pond turtle, Emys orbicularis: a secure but costly strategy? Biol Conserv 129: 236-243.
53. Schwartz TS, Osentoski M, Lamb T, Karl SA (2003) Microsatellite loci for the North American tortoises (genus Gopherus) and their applicability to other turtle species. Mol Ecol Notes 3: 283-286.
54. Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137: 1147-1155.
55. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19: 489-496.
56. Theissinger K, FitzSimmons N, Limpus C, Parmenter C, Phillott A (2009) Mating system, multiple paternity and effective population size in the endemic flatback turtle (Natator depressus) in Australia. Conserv Genet 10: 329-346.
57. Tuberville TD, Norton TM, Waffa BJ, Hagen C, Glenn TC (2011) Mating system in a gopher tortoise population established through multiple translocations: apparent advantage of prior residence. Biol Conserv 144: 175-183.
58. Turner FB, Hayden P, Burge BL, Roberson JB (1986) Egg production by the desert tortoise (Gopherus agassizii) in California. Herpetologica 42: 93-104.
59. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17: 2566-2580.
60. U. S. Fish Wildlife Service (1990) Endangered and threatened status for the Mojave population of the desert tortoise. Federal Register 55: 12178-12191.
61. U. S. Fish Wildlife Service (1994) Desert tortoise (Mojave population) recovery plan. U. S. Fish and Wildlife Service, Portland.
62. Valenzuela N (2000) Multiple paternity in side-neck turtles Podocnemis expansa: evidence from microsatellite DNA data. Mol Ecol 9: 99-105.
63. Zbinden JA, Largiader CR, Leippert F, Margaritoulis D, Arlettaz R (2007) High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Mol Ecol 16: 3703-3711.