Conservation Genetics

, Volume 10, Issue 2, pp 329–346 | Cite as

Mating system, multiple paternity and effective population size in the endemic flatback turtle (Natator depressus) in Australia

  • Kathrin Theissinger
  • N. N. FitzSimmons
  • C. J. Limpus
  • C. J. Parmenter
  • A. D. Phillott
Research article

Abstract

In recent years, genetic studies have been used to investigate mating systems of marine turtles, but to date no such research has been conducted on the flatback turtle (Natator depressus). This study investigates paternity of flatback turtle clutches at two rookeries in Queensland, Australia; Peak Island (Keppel Bay), and Mon Repos (Bundaberg). In the 2004–2005 nesting season, tissue samples were taken from either single or multiple clutches (n = 16) of nesting females (n = 8) representing a sampling effort ranging from 25% to 50% offspring per nest. Determination of the extent of multiple paternity was done using a comparative approach that included initial inferences based on observed alleles, Chi-square tests for deviations from Mendelian expectations, and three software programs (PARENTAGE1.0, GERUD2.0 and MER3.0). Results varied depending on the approach, but by calculating a consensus value of the output from these different methods, the null hypothesis of single paternity could be rejected in at least 11 of the 16 clutches (69%). Multiple paternity was thus observed in the clutches of six of nine females (67%), with two or three fathers being the most likely outcome. Analyses of successive clutches illustrated that paternal contribution to clutch fertilization can vary through time, as observed for two females. This first evidence regarding the mating system of flatback turtles indicates that multiple paternity is common in this species and that the observed frequency of multiple paternity is among the higher values reported in marine turtle species. Application of these results to estimates of effective population size (Ne) suggests that population size may have been relatively stable over long periods. Continued monitoring of population dynamics is recommended to ensure that future changes in the east coast can be detected.

Keywords

Marine turtles Microsatellites Conservation genetics Sperm storage and sperm competition 

References

  1. Aggarwal RK, Velavan TP, Udaykumar D, Hendre PS, Shanker K, Choudhury C, Singh L (2004) Development and characterization of novel microsatellite markers from the olive ridley sea turtle (Lepidochelys olivacea). Mol Ecol Notes 4:77–79CrossRefGoogle Scholar
  2. Allard MW, Miyamoto MM, Bjorndal KA, Bolten AB, Bowen BW (1994) Support for natal homing in green turtles from mitochondrial DNA sequences. Copeia 1994:34–41CrossRefGoogle Scholar
  3. Arnquist G (1989) Multiple mating in a water strider: mutual benefits or intersexual conflict? Anim Behav 38:749–756CrossRefGoogle Scholar
  4. Arnquist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164CrossRefGoogle Scholar
  5. Avens L, Braun-McNeill J, Epperly S, Lohman KJ (2003) Site fidelity and homing behavior in juvenile loggerhead turtles (Caretta caretta). Mar Biol 143:211–220CrossRefGoogle Scholar
  6. Avise JC (2004) Molecular markers, natural history and evolution, 2nd edn. Sinauer Associates, Inc. Publishers, SunderlandGoogle Scholar
  7. Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154CrossRefGoogle Scholar
  8. Balazs GH, Chaloupka M (2004) Thirty-year recovery trend in the once depleted Hawaiian green sea turtle stock. Biol Conserv 117:491–498CrossRefGoogle Scholar
  9. Barton NH, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409–415PubMedCrossRefGoogle Scholar
  10. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  11. Berry JF, Shine R (1980) Sexual size dimorphism and sexual selection in turtles (Order Chelonia). Oecologia 44:185–191CrossRefGoogle Scholar
  12. Birkhead T (2000) Promiscuity: an evolutionary history of sperm competition and sexual conflict. Faber and Faber, LondonGoogle Scholar
  13. Bjorndal KA, Jackson JBC (2003) Roles of sea turtles in marine ecosystems: reconstructing the past. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol 2. CRC Press, Boca Raton, pp 259–273Google Scholar
  14. Bollmer JL, Irwin ME, Rieder JP, Parker PG (1999) Multiple paternity in loggerhead turtle clutches. Copeia 1999:475–478CrossRefGoogle Scholar
  15. Booth J, Peters JA (1972) Behavioural study on the green turtle (Chelonia mydas) in the sea. Anim Behav 20:475–478CrossRefGoogle Scholar
  16. Bowen BW (1995) Tracking marine turtles with genetic markers. BioScience 45:528–534CrossRefGoogle Scholar
  17. Bowen BW, Bass AL, Chow SM, Bostrom M, Bjorndal KA, Bolten AB, Okuyama T, Bolker BM, Epperly S, Lacasella E, Shaver D, Dodd M, Hopkins-Murphy SR, Musick JA, Swingle M, Rankin-Baransky K, Teas W, Witzell WN, Dutton PH (2004) Natal homing in juvenile loggerhead turtles (Caretta caretta). Mol Ecol 13:3797–3808PubMedCrossRefGoogle Scholar
  18. Bretman A, Tregenza T (2005) Measuring polyandry in wild populations: a case study using promiscuous crickets. Mol Ecol 14:2169–2179PubMedCrossRefGoogle Scholar
  19. Byrne PG, Roberts JD (2000) Does multiple paternity improve fitness of the frog Crinia georgiana? Evolution 54:968–973PubMedGoogle Scholar
  20. Comuzzie DKL, Owens DW (1990) A quantitative analysis of courtship behavior in captive green turtles (Chelonia mydas). Herpetologica 46:195–202Google Scholar
  21. Crim JL, Spotila LD, Spotila JR, O’Connor M, Reina R, Williams CJ, Paladino FV (2002) The leatherback turtle, Dermochelys coriacea, exhibits both polyandry and polygyny. Mol Ecol 11:2097–2106PubMedCrossRefGoogle Scholar
  22. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New YorkGoogle Scholar
  23. Dethmers KEM, Broderick D, Moritz C, FitzSimmons NN, Limpus CJ, Lavery S, Whiting S, Guinea M, Prince RIT, Kennett R (2006) The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Mol Ecol 15:3931–3946PubMedCrossRefGoogle Scholar
  24. Dobson FS, Chesser RK, Hoogland JL, Sugg DW, Foltz DW (2004) The influence of social breeding groups on effective population size in black-tailed prairie dogs. J Mammal 85:58–66CrossRefGoogle Scholar
  25. Emery AM, Wilson IJ, Craig S, Boyle PR, Noble LR (2001) Assignment of paternity groups without access to parental genotypes: multiple mating and developmental plasticity in squid. Mol Ecol 10:1265–1278PubMedCrossRefGoogle Scholar
  26. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223PubMedCrossRefGoogle Scholar
  27. Ewing HE (1943) Continued fertility in female box turtles following mating. Copeia 1943:112–114CrossRefGoogle Scholar
  28. FitzSimmons NN (1998) Single paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas). Mol Ecol 7:575–584PubMedCrossRefGoogle Scholar
  29. FitzSimmons NN, Moritz C, Limpus CJ, Pope L, Prince R (1997) Geographic structure of mitochondrial and nuclear gene polymorphisms in Australian green turtle populations and male-biased gene flow. Genetics 147:1843–1854PubMedGoogle Scholar
  30. Frankham R (1995) Effective population size ratios in wildlife: a review. Genet Res 66:95–107Google Scholar
  31. Garant D, Dodson JJ, Bernatchez L (2001) A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.). J Hered 92:137–145PubMedCrossRefGoogle Scholar
  32. Gist DH, Congdon JD (1998) Oviductal sperm storage as a reproductive tactic of turtles. J Exp Zool 282:526–534PubMedCrossRefGoogle Scholar
  33. Gist DH, Jones JM (1989) Sperm storage within the oviduct of turtles. J Morphol 199:379–384CrossRefGoogle Scholar
  34. Godley BJ, Broderick AC, Frauenstein R, Glen F, Hays GC (2002) Reproductive seasonality and sexual dimorphism in green turtles. Mar Ecol Prog Ser 226:125–133CrossRefGoogle Scholar
  35. Groombridge B (1982) The IUCN Amphibia—Reptilia Red Data Book Part 1: Testudines, Crocodylia, Rhynchocephalia. IUCNGoogle Scholar
  36. Gullberg A, Olsson M, Tegelström H (1997) Male mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioural and molecular genetics data. Mol Ecol 6:105–112CrossRefGoogle Scholar
  37. Harry JL, Briscoe DA (1988) Multiple paternity in the loggerhead turtle (Caretta caretta). J Hered 79:96–99PubMedGoogle Scholar
  38. Hart A (2002) Fisheries monitoring programs in the Southern Gulf of Carpentaria—a review. Australian Centre for Tropical Freshwater ResearchGoogle Scholar
  39. Hasselquist D, Sherman PW (2001) Social mating systems and extrapair fertilizations in passerine birds. Behav Ecol 12:457–466CrossRefGoogle Scholar
  40. Heithaus MR, Frid A, Dill LM (2002) Shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles. Mar Biol 140:229–236CrossRefGoogle Scholar
  41. Hoeckert 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 89:107–113CrossRefGoogle Scholar
  42. Ireland JS, Broderick AC, Glen F, Godley BJ, Hays GC, Lee PLM, Skibinski DOF (2003) Multiple paternity assessed using microsatellite markers, in green turtles Chelonia mydas (Linnaeus, 1758) of Ascension Island, South Atlantic. J Exp Mar Biol Ecol 291:149–160Google Scholar
  43. Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429CrossRefGoogle Scholar
  44. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of genetic benefits. Biol Rev Camb Philos Soc 75:21–64PubMedCrossRefGoogle Scholar
  45. 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 15:2567–2575PubMedCrossRefGoogle Scholar
  46. Jessop TS, FitzSimmons NN, Limpus CJ, Whittier JM (1999) Interactions between behaviour and plasma steroids within the scramble mating system of the promiscuous green turtle, Chelonia mydas. Horm Behav 36:86–97PubMedCrossRefGoogle Scholar
  47. 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 84:520–526CrossRefGoogle Scholar
  48. Jones AG (2001) GERUD1.0: a computer program for the reconstruction of paternal genotypes from progeny arrays using multi-locus DNA data. Mol Ecol Notes 1:215–218CrossRefGoogle Scholar
  49. Jones AG (2005) GERUD2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Mol Ecol Notes 5:708–711CrossRefGoogle Scholar
  50. Kichler K, Holder MT, Davis SK, Márquez R, Owens DW (1999) Detection of multiple paternity in the Kemp’s ridley sea turtle with limited sampling. Mol Ecol 8:819–830CrossRefGoogle Scholar
  51. Lahanas PN, Miyamoto MM, Bjorndal KA, Bolten AB (1994) Molecular evolution and population genetics of Greater Caribbean green turtles (Chelonia mydas) as inferred from mitochondrial DNA control region sequences. Genetica 94:57–66PubMedCrossRefGoogle Scholar
  52. Laurent L, Casale P, Bradai M, Godley BJ, Gerosa G, Broderick AC, Schroth W, Schierwater B, Levy AM, Freggi D, Abd El-Mawla EM, Hadoud DA, Gomati HE, Domingo M, Hadjichristophorou M, Kornaraky L, Demirayak F, Gautier CH (1998) Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol Ecol 7:1529–1542PubMedCrossRefGoogle Scholar
  53. Lee PLM, Hays GC (2004) Polyandry in marine turtles: females make the best of a bad job. Proc Natl Acad Sci USA 101:6530–6535PubMedCrossRefGoogle Scholar
  54. Legge S, Cockburn A (2000) Social and mating system of cooperatively breeding laughing kookaburras (Dacelo novaeguineae). Behav Ecol Sociobiol 47:220–229CrossRefGoogle Scholar
  55. Limpus CJ (1993) The green turtle (Chelonia mydas) in Queensland: breeding males in the southern Great Barrier Reef. Wildl Res 20:513–523CrossRefGoogle Scholar
  56. Limpus CJ (1997) Summary of the biology of marine turtles in Australia. QLD Dept EnvironmentGoogle Scholar
  57. Limpus CJ (2007) A biological review of Australian Marine turtles. 5. Flatback Turtle Natator depressus (Garman). Queensland Environmental Protection Agency, BrisbaneGoogle Scholar
  58. Limpus CJ, Baker V, Miller JD (1979) Movement induced mortality of loggerhead eggs. Herpetologica 35:335–338Google Scholar
  59. Limpus CJ, Fleay A, Baker V (1984) The flatback turtle, Chelonia depressa, in Queensland: reproductive periodicity, philopatry and recruitment. Aust Wildl Res 11:579–587CrossRefGoogle Scholar
  60. Limpus CJ, Miller JD, Parmenter CJ, Reimer D, McLachlan N, Webb R (1992) Migration of green (Chelonia mydas) and loggerhead (Caretta caretta) turtles to and from the eastern Australian rookeries. Wildl Res 19:347–357CrossRefGoogle Scholar
  61. Limpus CJ, Parmenter CJ, Limpus DJ (2002) The status of the flatback turtle, Natator depressus, in eastern Australia. In: Mosier A, Foley A, Borst, B (compilers). Proceedings of the twentieth annual symposium on sea turtle biology and conservation. NOAA Tech. Memo. NMFS-SEFSC-477, pp 140–142Google Scholar
  62. Limpus CJ, McLaren M, McLaren G, Knuckey B (2006) Queensland turtle conservation project: Curtis Island and Woongarra Coast flatback turtle studies, 2005–2006. Conservation technical and data report, vol 2006(4). Queensland Environmental Protection AgencyGoogle Scholar
  63. Luschi P, Hays GC, Del Seppia C, Marsh R, Papi F (1998) The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry. Proc R Soc Lond B 265:2279–2284CrossRefGoogle Scholar
  64. Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently? Nature 355:440–441CrossRefGoogle Scholar
  65. Madsen T, Ujvari B, Olsson M, Shine R (2005) Paternal alleles enhance female reproductive success in tropical pythons. Mol Ecol 14:1783–1787PubMedCrossRefGoogle Scholar
  66. Marcovaldi MA, Marcovaldi GG (1999) Marine turtles of Brazil: the history and structure of Projeto TAMAR-IBAMA. Biol Conserv 91:35–41CrossRefGoogle Scholar
  67. Matocq MD (2004) Reproductive success and effective population size in wood rats (Neotoma macrotis). Mol Ecol 13:1635–1642PubMedCrossRefGoogle Scholar
  68. Moore MK, Ball RM (2002) Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis. Mol Ecol 11:281–288PubMedCrossRefGoogle Scholar
  69. Musick JA (1999) Ecology and conservation of long-lived marine animals. Am Fish Soc Symp 23:1–10Google Scholar
  70. Newcomer SD, Zeh JA, Zeh DW (1999) Genetic benefits enhance the reproductive success of polyandrous females. Proc Natl Acad Sci USA 96:10236–10241PubMedCrossRefGoogle Scholar
  71. Nievergelt CM, Mutschler T, Feistner AT, Woodruff DS (2002) Social system of the Alaotran gentle lemur (Hapalemur griseus alaotrensis): genetic characterization of group composition and mating system. Am J Primatol 57:157–176PubMedCrossRefGoogle Scholar
  72. Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341CrossRefGoogle Scholar
  73. Nunney L, Elam DR (1994) Estimating the effective population size of conserved populations. Conserv Biol 8:175–184CrossRefGoogle Scholar
  74. Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204CrossRefGoogle Scholar
  75. Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Moeller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 503–577CrossRefGoogle Scholar
  76. Owens DW, Morris YA (1985) The comparative endocrinology of sea turtles. Copeia 1985:723–735CrossRefGoogle Scholar
  77. Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65PubMedCrossRefGoogle Scholar
  78. Parmenter CJ (1980) Incubation of the eggs of the green sea turtle, Chelonia mydas, in Torres Strait, Australia: the effect of movement on hatchability. Aust Wildl Res 7:487–491CrossRefGoogle Scholar
  79. Parmenter CJ (1993) A preliminary evaluation of the performance of passive integrated transponders and metal tags in a population study of the flatback sea turtle (Natator depressus). Wildl Res 20:375–381CrossRefGoogle Scholar
  80. Parmenter CJ (1994a) Australian sea turtle research, conservation and management: a 1993 status review. In: Lunney D, Ayers D (eds) Herpetology in Australia: a diverse discipline. Royal Society of New South Wales, Sydney, pp 321–325Google Scholar
  81. Parmenter CJ (1994b) Species review: the flatback turtle—Natator depressa. In: James R (ed) Proceedings of the Australian marine turtle conservation workshop, Qld Dept Environm Her, Aust Nat Conserv Agen, QLD, Australia, pp 60–62Google Scholar
  82. Parmenter CJ (2003) Plastic flipper tags are inadequate for long-term identification of the flatback sea turtle (Natator depressus). Wildl Res 30:519–521CrossRefGoogle Scholar
  83. Parmenter CJ, Limpus CJ (1995) Female recruitment, reproductive longevity and inferred hatchling survivorship for the flatback turtle (Natator depressus) at a major eastern Australian rookery. Copeia 1995:474–477CrossRefGoogle Scholar
  84. Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage and genetic paternity. J Hered 92:206–211PubMedCrossRefGoogle Scholar
  85. Pearse DE, Janzen FJ, Avise JC (2001) Genetic markers substantiate long-term storage and utilization of sperm by female painted turtles. Heredity 86:378–384PubMedCrossRefGoogle Scholar
  86. 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 51:164–171CrossRefGoogle Scholar
  87. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  88. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  89. Pitcher TE, Neff BD, Rodd FH, Rowe L (2003) Multiple mating and sequential mate choice in guppies: females trade up. Biol Sci 270:1623–1629CrossRefGoogle Scholar
  90. Poiner IR, Buckworth RC, Harris ANM (1990) Incidental capture and mortality of sea turtles in Australia’s northern prawn fishery. Aust J Mar Freshw Res 41:97–110CrossRefGoogle Scholar
  91. Polovina JJ, Kobayashi DR, Parker DM, Seki MP, Balasz GH (2000) Turtles on the edge: movement of loggerhead turtles (Caretta caretta) along oceanic fronts, spanning longline fishing grounds in the central North Pacific, 1997–1998. Fish Oceanogr 9:71–82CrossRefGoogle Scholar
  92. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9221PubMedCrossRefGoogle Scholar
  93. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  94. Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the co-ancestry coefficient: basis for a short-term genetic distance. Genetics 105:767–779PubMedGoogle Scholar
  95. Rodríguez-Teijeiro JD, Puigcerver M, Gallego S, Cordero PJ, Parkin DT (2003) Pair bonding and multiple paternity in the polygamous common quail Coturnix coturnix. Ethology 109:291–302CrossRefGoogle Scholar
  96. Roques S, Díaz-Paniaqua C, Andreu AC (2004) Microsatellite markers reveal multiple paternity and sperm storage in the Mediterranean spur thighed tortoise, Testudo graeca. Can J Zool 82:153–159CrossRefGoogle Scholar
  97. Roques S, Díaz-Paniaqua 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 129:236–243CrossRefGoogle Scholar
  98. Sahertian IH, Noija DJ (1994) Pilot study on the ecology and management of green turtles in the conservation area of South East Aru (Aru Islands-Moluccas). Pattimura University, AmbonGoogle Scholar
  99. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver.2.000: a software for population genetic data analyses. Genetics Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  100. Seminoff JA, Jones TT (2006) Diet movements and activity ranges of green turtles (Chelonia mydas) at a temperate foraging area in the Gulf of California, Mexico. Herpetol Conserv Biol 1:81–86Google Scholar
  101. Sever DM, Hamlett WC (2002) Female sperm storage in reptiles. J Exp Zool 292:187–199PubMedCrossRefGoogle Scholar
  102. Stockley P, Searle JB, Mcdonald DW, Jones CS (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B 254:173–179CrossRefGoogle Scholar
  103. Sugg DW, Chesser RK (1994) Effective population sizes with multiple mating. Genetics 137:1147–1155PubMedGoogle Scholar
  104. Swartz Soukup S, Thompson C (1998) Social mating system and reproductive success in house wrens. Behav Ecol 9:43–48CrossRefGoogle Scholar
  105. Troëng S, Rankin E (2005) Long-term conservation efforts contribute to positive green turtle Chelonia mydas nesting trend at Tortuguero, Costa Rica. Biol Conserv 121:111–116CrossRefGoogle Scholar
  106. Ulrich GF, Parkes AS (1978) The green sea turtle (Chelonia mydas): further observations on breeding in captivity. J Zool 185:237–251CrossRefGoogle Scholar
  107. van Camp LM, Donnellan SC, Dyer AR, Fairwaether PG (2004) Multiple paternity in field- and captive-laid egg strands of Sepiotheutis australis (Cephalopoda: Loliginidae). Mar Freshw Res 55:819–823CrossRefGoogle Scholar
  108. Wang J (2004) Estimating pairwise relatedness from dominant genetic markers. Mol Ecol 13:3169–3178PubMedCrossRefGoogle Scholar
  109. Westneat DF, Frederick PC, Haven Wiley R (1987) The use of genetic markers to estimate the frequency of successful alternative reproductive tactics. Behav Ecol Sociobiol 21:35–45CrossRefGoogle Scholar
  110. Westneat JH, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369Google Scholar
  111. Zbinden JA, Largiader AR, Leippert F, Margaritoulis D, Arlettaz R (2007) High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Mol Ecol 16:3703–3711PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Kathrin Theissinger
    • 1
    • 2
  • N. N. FitzSimmons
    • 2
  • C. J. Limpus
    • 3
  • C. J. Parmenter
    • 4
  • A. D. Phillott
    • 4
    • 5
  1. 1.Institute of Molecular EcologyJohannes Gutenberg UniversityMainzGermany
  2. 2.Institute for Applied EcologyUniversity of CanberraCanberraAustralia
  3. 3.Environmental Protection AgencyBrisbaneAustralia
  4. 4.School of Biological and Environmental SciencesCentral Queensland UniversityRockhamptonAustralia
  5. 5.School of Veterinary and Biomedical SciencesJames Cook UniversityTownsvilleAustralia

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