Abstract
Variation in levels of multiple paternity (MP) among species, populations and individuals has important ecological and evolutionary ramifications including maintenance of genetic diversity and offspring fitness benefits. Within species, differences in breeding experience and body size may affect the levels of MP via mate choice preferences. The present study tested these ideas in an Australian loggerhead turtle (Caretta caretta) population at Mon Repos Beach (24°48°S, 152°27°E, Queensland) to determine if variation in MP was related female breeding history or body size, or influenced embryo and hatchling outcomes in clutches from 29 females and 552 hatchlings. MP was moderately high (65.5%), but experienced females did not have higher levels of MP than first-time breeders (neophytes), nor was female size related to the number of sires. Instead, more subtle patterns emerged: multiply sired clutches of experienced females were sired by more males than those of multiply sired neophyte clutches and primary fathers sired a greater proportion of offspring when mated to larger females. These findings are consistent with cross-seasonal sperm storage in experienced breeders contributing to a small proportion of paternity and size-dependent variation in polyandrous mating behaviour. MP did not influence offspring size, levels of within-clutch morphological variation or hatching success. However, the number of sires of a clutch was positively correlated with proportion of developed embryos, suggesting a fitness advantage of MP. From a population perspective, male-biased sex ratios likely contribute to the MP levels observed, and levels could decrease with projected feminisation of populations due to climate change.
Similar content being viewed by others
References
Adams EM, Jones AG, Arnold SJ (2005) Multiple paternity in a natural population of a salamander with long-term sperm storage. Mol Ecol 14:1803–1810. https://doi.org/10.1111/j.1365-294X.2005.02539.x
Alfaro-Núñez A, Jensen MP, Abreu-Grobois FA (2015) Does polyandry really pay off? The effects of multiple mating and number of fathers on morphological traits and survival in clutches of nesting green turtles at Tortuguero. PeerJ. https://doi.org/10.7717/peerj.880
Banger N (2012) Consequences of multiple paternity for female fitness in an Ontario population of northern map turtles, Graptemys geographica. Master Thesis. University of Ottawa, Ottawa
Barry F, Weatherhead P, Philipp D (1992) Multiple paternity in a wild population of northern water snakes, Nerodia sipedon. Behav Ecol Sociobiol 30:193–199. https://doi.org/10.1007/BF00166703
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368. https://doi.org/10.1038/hdy.1948.21
Bates D, Maechler M, Bolker B (2011) Lme4: linear mixed-effect models using s4 classes. http://cran.R-project.org/package=lme4. R package version 0.999375-42
Birkhead TR, Moller AP (1993) Sexual selection and the temporal separation of reproductive events-sperm storage data from reptiles, birds and mammals. Biol J Linn Soc 50:295–311. https://doi.org/10.1111/j.1095-8312.1993.tb00933.x
Birkhead TR, Moller AP (1998) Sperm competition and sexual selection. Academic Press, San Diego
Bolten AB (1999) Techniques for measuring turtles. In: Donnelly M, Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M (eds) Research for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group, Washington, DC, pp 110–114
Booth J, Peters JA (1972) Behavioural studies on the green turtle (Chelonia mydas) in the sea. Anim Behav 20:808–812. https://doi.org/10.1016/S0003-3472(72)80155-6
Booth DT, Burgess E, McCosker J, Lanyon JM (2005) The influence of incubation temperature on post-hatching fitness characteristics of turtles. Int Congr Ser 1275:226–233. https://doi.org/10.1016/j.ics.2004.08.057
Boyle M, Hone J, Schwanz LE, Georges A (2014) Under what circumstances do climate-driven sex ratios enhance versus diminish population persistence? Ecol Evol 4:4522–4533. https://doi.org/10.1002/ece3.1316
Broderick AC, Glen F, Godley BJ, Hays GC (2003) Variation in reproductive output of marine turtles. J Exp Mar Biol Ecol 288:95–109. https://doi.org/10.1016/S0022-0981(03)00003-0
Calsbeek R, Sinervo B (2004) Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild. J Evol Biol 17:464–470. https://doi.org/10.1046/j.1420-9101.2003.00665.x
Campbell CL, Lagueux CJ (2005) Survival probability estimates for large juvenile and adult green turtles (Chelonia mydas) exposed to an artesanal marine turtle fishery in the Western Caribbean. Herpetologica 61:91–103. https://doi.org/10.1655/04-26
Cardona L, Clusa M, Eder E, Demetropoullos A, Margaritoulis D, Rees A, Hamza AA, Khali M, Levy Y, Tükozan O, Marín I, Auilar A (2014) Distribution patterns and foraging ground productivity determine clutch size in Mediterranean loggerhead turtles. Mar Ecol Prog Ser 497:229–241. https://doi.org/10.3354/meps10595
Chen S, Zhang L, Le Y, Waqas Y, Chen W, Zhang Q, Ullah S, Liu T, Hu L, Li Q, Yang P (2015) Sperm storage and spermatozoa interaction with epithelial cells in oviduct of Chinese soft-shelled turtles, Pelodiscus sinensis. Ecol Evol 5:3023–3030. https://doi.org/10.1002/ece3.1575
Chu CT, Booth DT, Limpus CJ (2008) Estimating the sex ratio of loggerhead turtle hathclings at Mon Repos rookery (Australia) from nest temperatures. Aust J Zool 56:57–64. https://doi.org/10.1071/ZO08004
Coleman SW, Jones AG (2011) Patterns of multiple paternity and maternity in fishes. Biol J Linn Soc 103:735–760. https://doi.org/10.1111/j.1095-8312.2011.01673.x
Comuzzie DKC, Owens DW (1990) A quantitative analysis of courtship behavior in captive green sea turtles (Chelonia mydas). Herpetologica 46:195–202. http://www.jstor.org/stable/3892904
Crawley MJ (2007) The R book. Wiley, Chichester
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 11:2097–2106. https://doi.org/10.1046/j.1365-294X.2002.01591.x
Dalleau M, Ciccione S, Mortimer JA, Garnier J, Benhamou S, Bourjea J (2012) Nesting phenology of marine turtles: insights from a regional comparative analysis on green turtle (Chelonia mydas). PLoS One 7:e46920. https://doi.org/10.1371/journal.pone.0046920
Duran N, Dunbar SG, Escobar RA III, Standish TG (2015) High frequency of multiple paternity in a solitary population of olive ridley sea turtles in Honduras. J Exp Mar Biol Ecol 463:63–71. https://doi.org/10.1016/j.jembe.2014.10.023
Emlen ST, Oring LW (1977) Ecology, sexual selection, and evolution of mating systems. Science 197:215–223. https://doi.org/10.1126/science.327542
Ewing HE (1943) Continued fertility in female box turtle following mating. Copeia 1943:112–114. http://www.jstor/stable/1437776
FitzSimmons NN (1998) Single paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas). Mol Ecol 7:575–584. https://doi.org/10.1046/j.1365-294x.1998.00355.x
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. https://doi.org/10.1093/oxfordjournals.molbev.a040218
FitzSimmons NN, Limpus CJ, Norman JA, Goldizen AR, Miller JD, Moritz C (1997) Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proc Nat Acad Sci USA 94:8912–8917. https://doi.org/10.1073/pnas.94.16.8912
Frick MG, Slay CK, Quinn CA, Windham-Reid A, Duley PA, Ryder CM, Morse LJ (2000) Observations of courtship behavior in loggerhead sea turtles (Caretta caretta) from southeastern Georgia and northwestern Florida. J Herpetol 34:153–158. http://www.jstor.org/stable/1565255
Fuentes MMPB, Hamann M, Limpus CJ (2010) Past, current and future thermal profiles of green turtle nesting grounds: implications from climate change. J Exp Mar Biol Ecol 383:56–64. https://doi.org/10.1016/j.jembe.2009.11.003
Gist DH, Congdon JD (1998) Oviductal sperm storage as a reproductive tactic of turtles. J Exp Zool 282:526–534. https://doi.org/10.1002/(SICI)1097-010X(199811/12)282:4/53.3.CO;2-Q
Gyuris E (2000) The relationship between body size and predation rates of hatchling green turtles (Chelonia mydas): Is bigger better? In: Pilcher N, Ismail G (eds) Sea turtles of the Indo-Pacific: research management and conservation. Academic Press, New York, pp 143–147
Harry JL, Briscoe DA (1988) Multiple paternity in the loggerhead turtle (Caretta caretta). J Hered 79:96–99. https://doi.org/10.1093/oxfordjournals.jhered.a110480
Hatase H, Omuta K, Komatsu T (2015) Loggerhead turtle (Caretta caretta) offspring size does not vary with maternal alternative foraging behaviors: support for their phenotypic plasticity. Mar Biol 162:1567–1578. https://doi.org/10.1007/s00227-015-2693-x
Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2007) Investigating the potential impacts of climate change on a marine turtle population. Glob Chang Biol 13:923–932. https://doi.org/10.1111/j.1365-2486.2006.01320.x
Hays GC, Fossette S, Katselidis KA, Schofield G, Gravenor MB (2010) Breeding periodicity for male sea turtles, operational sex ratios, and implications in the face of climate change. Conserv Biol 24:1636–1643. https://doi.org/10.1111/j.1523-1739.2010.01531.x
Heithaus MR, Frid A, Wirsing AJ, Bejder Dill LM (2005) Biology of sea turtles under risk from tiger sharks at a foraging ground. Mar Ecol Prog Ser 288:285–294. https://doi.org/10.3354/meps288285
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. https://doi.org/10.1038/sj.hdy.6800103
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 291:149–160. https://doi.org/10.1016/S0022-0981(03)00118-7
Janzen FJ, Tucker JK, Paukstis GL (2000) Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81:2290–2304. https://doi.org/10.1890/0012-9658(2000)081[2290:EAOAEL]2.0.CO;2
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64. https://doi.org/10.1111/j.1469-185X.1999.tb00040.x
Jensen MP, Abreu-Grobois FA, FrydHayenberg 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. https://doi.org/10.1111/j.1365-294X.2006.02951.x
Jensen MP, FitzSimmons NN, Dutton PH (2013) Molecular genetics of sea turtles. In: Wyneken J, Lohmann KJ, Musick JA (eds) Biology of the sea turtles, vol 3. CRC Press, Boca Raton, pp 135–161
Jessop TS, FitzSimmons NN, Limpus CJ, Whittier JM (1999) Interactions between behavior and plasma steriods within the scramble mating system of the promiscuous green turtle, Chelonia mydas. Horm Behav 36:86–97. https://doi.org/10.1006/hbeh.1999.1527
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 Note 5:708–711. https://doi.org/10.1111/j.1471-8286.2005.01029.x
Jones OR, Wang J (2010) Colony: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. https://doi.org/10.1111/j.1755-0998.2009.02787.x
Joseph J, Shaw PW (2011) Multiple paternity in egg clutches of hawksbill turtles (Eretmochelys imbricata). Conserv Genet 12:601–605. https://doi.org/10.1007/s10592-010-0168-7
Kichler K, Holder MT, Davis SK, Marquez R, Owens DW (1999) Detection of multiple paternity in the Kemp’s ridley sea turtle with limited sampling. Mol Ecol 8:819–830. https://doi.org/10.1046/j.1365-294X.1999.00635.x
Lasala JA, Harrison JS, Williams KL, Rostal DC (2013) Strong male-biased operational sex ratio in a breeding population of loggerhead turtles (Caretta caretta) inferred by paternal genotype reconstruction analysis. Ecol Evol 3:4736–4747. https://doi.org/10.1002/ece3.761
LeBlanc AM, Rostal DC, Drake KK, Williams KL, Frick MG, Robinette J, Barnard-Keinath DE (2014) The influence of maternal size on the eggs and hatchlings of loggerhead sea turtles. Southeast Nat 13:587–599. https://doi.org/10.1656/058.013.0318
Lee PLM, Hays GC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proc Nat Acad Sci USA 101:6530–6535. https://doi.org/10.1073/pnas.0307982101
Lehikoinen A, Christensen TK, Öst KC, Kilpi M, Saurola P, Vattulainen A (2008) Large-scale change in sex ratio of a declining eider Somateria mollissima population. Wildl Biol 14:288–301. https://doi.org/10.2981/0909-6396(2008)14[288:LCITSR]2.0.CO;2
Limpus CJ (1985) A study of the loggerhead turtle, Caretta caretta, in Queensland. Dissertation. University of Queensland, Queensland
Limpus CJ (1993) The green turtle, Chelonia mydas, in Queensland: breeding males in the southern Great Barrier Reef. Wildl Res 20:513–523. https://doi.org/10.1071/WR9930513
Limpus CJ (1996) Changing fecundity with age in Queensland Caretta caretta. In: Keinath JA, Barnard DE, Musick JA, Bell CD (eds) Proceedings of the fifteenth annual symposium on sea turtle biology and conservation, NOAA technical memorandum NMFS-SEFSC-387, pp 167–169
Limpus CJ (2008) A biological review of Australian marine turtles species. 1. Loggerhead turtle, Caretta caretta (Linnaeus). State of Queensland, Environmental Protection Agency, Brisbane
Limpus CJ, Limpus DJ (2003a) Biology of the loggerhead turtle in western South Pacific Ocean foraging areas. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution, Washington, DC, pp 93–113
Limpus CJ, Limpus DJ (2003b) Loggerhead turtles in the equatorial and southern Pacific Ocean: a species in decline. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution, Washington, DC, pp 199–209
Limpus CJ, Couper PJ, Read MA (1994) The loggerhead turtle, Caretta caretta, in Queensland: population structure in a warm temperate feeding area. Mem Qld Mus 37:195–204
Lodé T, Holveck M-J, Lesbarréres D (2005) Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biol J Linn Soc 86:191–200. https://doi.org/10.1111/j.1095-8312.2005.00521.x
Magnhagen C (1991) Predation risk as a cost of reproduction. Trends Ecol Evol 6:183–186. https://doi.org/10.1016/0169-5347(91)90210-O
Miller JD (1985) Embryology of marine turtles. In: Gans C, Billett F, Maderson PFA (eds) Biology of the reptilia, vol 14. Academic Press, New York, pp 269–328
Miller JD, Limpus CJ, Godfrey MH (2003) Nest site selection, oviposition, eggs, development, hatching and emergence of loggerhead turtles. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution, Washington, DC, pp 125–143
Neff BD, Pitcher TE (2002) Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J Fish Biol 61:739–750. https://doi.org/10.1111/j.1095-8649.2002.tb00908.x
Nielsen JT (2010) Population structure and the mating system of loggerhead turtles (Caretta caretta). Dissertations. University of Miami, Coral Gables
Olsson M, Madsen T, Shine R (1997) Is sperm really so cheap? Cost of reproduction in male adders, Vipera berus. Proc R Soc B Biol Sci 264:455–459. https://doi.org/10.1098/rspb.1997.0065
Palmer KS, Rostal DC, Grumbles JS, Mulvey M (1998) Long-term sperm storage in the desert tortoise (Gopherus agassizii). Copeia 1998:702–705. https://doi.org/10.2307/1447800
Payne NL, Gillanderts BM, Semmens J (2011) Breeding durations as estimators of adult sex ratios and population size. Oecologia 165:341–347. https://doi.org/10.1007/s00442-010-1729-7
Pearse DE, Anderson EC (2009) Multiple paternity increases effective population size. Mol Ecol 18:3124–3127. https://doi.org/10.1111/j.1365-294X.2009.04268.x
Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage, and genetic paternity. J Hered 92:206–211. https://doi.org/10.1093/jhered/92.2.206
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. https://doi.org/10.1046/j.1365-2540.2001.00841.x
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. https://doi.org/10.1007/s00265-001-0421-7
Phillips KP, Jorgensen TH, Jolliffe KG, Jolliffe S-M, Henwood J, Richardson DS (2013) Reconstructing paternal genotypes to infer patterns of sperm storage and sexual selection in the hawksbill turtle. Mol Ecol 22:2301–2312. https://doi.org/10.1111/mec.12235
Pinckney J (1990) Correlation analysis of adult female, egg and hatchling sizes in the loggerhead turtle, Caretta caretta (L), nesting at Kiawah Island, South Carolina, USA. Bull Mar Sci 47:670–679
Read T, Booth DT, Limpus CJ (2013) Effect of nest temperature on hatchling phenotype of loggerhead turtles (Caretta caretta) from two South Pacific rookeries, Mon Repos and La Roche Perc. Aust J Zool 60:402–411. https://doi.org/10.1071/ZO12079
Real KM, Schmidt DJ, Hughes JM (2009) Mogurnda adspersa microsatellite markers: multiplexing and multi-tailed primer tagging. Conserv Genet Resour 1:411–414. https://doi.org/10.1007/s12686-009-9095-7
Rousset F (2008) Genepop ‘ 007: a complete re-implementation of the genepop software for windows and linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Sakaoka K, Yoshii M, Nakamura H, Kureha K, Uchida I (2007) Quantitative analysis of reproductive behavior in captive loggerhead turtles (Caretta caretta). Herpetol Rev 38:395–399
Sakaoka K, Yoshii M, Okamoto H, Sakai F, Nagasawa K (2011) Sperm utilization patterns and reproductive success in captive loggerhead turtles (Caretta caretta). Chelonian Conserv Biol 10:62–72. https://doi.org/10.2744/CCB-0878.1
Sarkar S, Sarkar NK, Maiti BR (2003) Oviductal sperm storage structure and their changes during the seasonal (dissociated) reproductive cycle in the soft-shelled turtle Lissemys punctata punctata. J Exp Zool 295A:83–91. https://doi.org/10.1002/jez.a.10135
Schofield G, Lilley MKS, Bishop CM, Brown P, Katseidis KA, Dimopoulos P, Pantis JD, Hays GC (2010) Conservation hotspots: implications of intense spatial area use by breeding male and female loggerheads at the Mediterranean’s largest rookery. Endanger Species Res 10:191–202. https://doi.org/10.3354/esr00137
Shamblin BM, Faircloth BC, Dodd M, Wood-Jones A, Castleberry SB, Carroll JP, Nairn CJ (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Mol Ecol Note 7:784–787. https://doi.org/10.1111/j.1471-8286.2007.01701.x
Shuster SM (2009) Sexual selection and mating systems. Proc Nat Acad Sci USA 106:1009–1016. https://doi.org/10.1073/pnas.0901132106
Simons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36:125–146. https://doi.org/10.1146/annurev.ecolsys.36.102403.112501
Sokal R, Michener C (1958) A statistical method for evaluating systematic relationships. University of Kansas Sci Bull 38:1409–1438
Sorin AB (2004) Paternity assignment for white-tailed deer (Odocoileus virginianus): mating across age classes and multiple paternity. J Mammal 85:356–362. https://doi.org/10.1644/1545-1542(2004)085<0356:PAFWDO>2.0.CO;2
Soulsbury CD (2010) Genetic patterns of paternity and testes size in mammals. PLoS One 5:A152–A157. https://doi.org/10.1371/journal.pone.0009581
Squires ZE, Wong BBM, Norman MD, Stuart-Fox D (2012) Multiple fitness benefits of polyandry in a cephalopod. PLoS One 7:e37074. https://doi.org/10.1371/journal.pone.0037074
Steifetlen O, Dale S (2006) Viability of an endangered population of ortolan buntings: the effect of a skewed operational sex ratio. Biol Conserv 132:88–97. https://doi.org/10.1016/j.biocon.2006.03.016
Stewart KR, Dutton PH (2011) Paternal genotype reconstruction reveals multiple paternity and sex ratios in a breeding population of leatherback turtles (Dermochelys coriacea). Conserv Genet 12:1101–1113. https://doi.org/10.1007/s10592-011-0212-2
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R.project.org/
Tedeschi JN, Mitchell NJ, Berry O, Whiting S, Meekan M, Kennington WJ (2014) Reconstructed paternal genotypes reveal variable rates of multiple paternity at three rookeries of loggerhead sea turtles (Caretta caretta) in Western Australia. Aust J Zool 62:454–462. https://doi.org/10.1071/ZO14076
Theissinger K, FitzSimmons NN, Limpus CJ, Parmenter CJ, Phillott AD (2009) Mating system, multiple paternity and effective population size in the endemic flatback turtle (Natator depressus) in Australia. Conserv Genet 10:329–346. https://doi.org/10.1007/s10592-008-9583-4
Tiwari M, Bjorndal KA (2000) Variation in morphology and reproduction in loggerheads, Caretta caretta, nesting in the United States, Brazil, and Greece. Herpetologica 56:343–356. http://www.jstor.org/stable/3893411
Tucker AD (2010) Nest site fidelity and clutch frequency of loggerhead turtles are better elucidated by satellite telemetry than by nocturnal tagging efforts: implications for stock estimation. J Exp Mar Biol Ecol 383:48–55. https://doi.org/10.1016/j.jembe.2009.11.009
Tucker AD, Frazer NB (1991) Reproductive variation in leatherback turtles, Dermochelys coriacea, at Culebra National Wildlife Refuge, Puerto Rico. Herpetologica 47:115–124. http://www.jstor.org/stable/3892822
Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580. https://doi.org/10.1111/j.1365-294X.2008.03772.x
Uller T, Schwartz T, Koglin T, Olsson M (2013) Sperm storage and sperm competition across ovarian cycles in the dragon lizard, Ctenophorus fordi. J Exp Zool Part A Ecol Genet Physiol 319:404–408. https://doi.org/10.1002/jez.1803
Van Buskirk J, Crowder LB (1994) Life-history variation in marine turtles. Copeia 1994:66–81. https://doi.org/10.2307/1446672
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Note 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320. https://doi.org/10.1016/S0169-5347(02)02533-8
Weir LK, Grant JWA, Hutchings JA (2011) The influence of operational sex ratio on the intensity of competition for mates. Am Nat 177:167–176. https://doi.org/10.1086/657918
Wells CP, Tomalty KM, Floyd CH, McElreath MB, May BP, Van Vuren DH (2017) Determinants of multiple paternity in a fluctuating population of ground squirrels. Behav Ecol Sociobiol 71:42. https://doi.org/10.1007/s/00265-017-2270-z
Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215. https://doi.org/10.1007/s002650050381
Weston Glenn JL, Civitello DJ, Lance SL (2009) Multiple paternity and kinship in the gray fox (Urocyon cinereoargenteus). Mamm Biol Z Säugetierkd 74:394–402. https://doi.org/10.1016/j.mambio.2008.10.003
Whiting AU, Chaloupka M, Limpus CJ (2008) Sampling error for hatchling turtle measurements: probing a rule-of-thumb. Copeia 2008:889–896. https://doi.org/10.1643/CH-07-194
Wibbels T, Owens DW, Limpus CJ, Reed PC, Amoss MS (1990) Seasonal changes in serum gonadal steroids associated with migration, mating and nesting in loggerhead sea turtle (Caretta caretta). Gen Comp Endocrinol 79:154–164. https://doi.org/10.1016/0016-6480(90)90099-8
Woolgar L, Trocini S, Mitchell N (2013) Key parameters describing temperature-dependent sex determination in the southernmost population of loggerhead sea turtles. J Exp Mar Biol Ecol 449:77–84. https://doi.org/10.1016/j.jembe.2013.09.001
Wright LI, Stokes KL, Fuller WJ, Godley BJ, McGowan A, Snape R, Tregenza T, Broderick AC (2012) Turtle mating patterns buffer against disruptive effects of climate change. Proc R Soc B 279:2122–2127. https://doi.org/10.1098/rspb.2011.2285
Wright LI, Fuller WJ, Godley BJ, McGowan A, Tregenza T, Broderick AC (2013) No benefits of polyandry to female green turtles. Behav Ecol 24:1022–1029. https://doi.org/10.1093/beheco/art003
Xiangkun H, Li Z, Meiying L, Huijun B, Nainan H, Qiusheng C (2008) Seasonal changes of sperm storage and correlative structures in male and female soft-shelled turtles, Trionyx sinensis. Anim Reprod Sci 108:435–445. https://doi.org/10.1016/j.anireprosci.2007.09.011
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 16:3703–3711. https://doi.org/10.1111/j.1365-294X.2007.03426.x
Acknowledgements
We thank the many volunteers of the turtle research program and the staff at Mon Repos Conservation Park for helping with the considerable logistics of the fieldwork. In particular, thanks to Helen Twaddle, the Limpus family, Kate Winter, Katherine Roberston and John Sergeev. We thank the Queensland Department of Environment and Heritage Protection for supporting the marine turtle research and monitoring. For helpful advice and support in the lab we thank Sophie Olsson-Pons and Nick Clark. Support for the project was provided through the Griffith School of Environment and the Environmental Futures Centre. We thank the anonymous reviewers of this manuscript for their constructive criticisms and helpful comments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Human and animal ethics
Animal use in this study was conducted in conjunction with research and monitoring by the Queensland Department of Environment and Heritage Protection under their wildlife use and animal ethics permit.
Additional information
Responsible Editor: P. Casale.
Reviewed by C. Carreras and B. I. González-Garza.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Howe, M., FitzSimmons, N.N., Limpus, C.J. et al. Multiple paternity in a Pacific marine turtle population: maternal attributes, offspring outcomes and demographic inferences. Mar Biol 165, 2 (2018). https://doi.org/10.1007/s00227-017-3258-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3258-y