High incidence of multiple paternity in an Australian snapping turtle (Elseya albagula)
Erica V. Todd A D , David Blair A , Colin J. Limpus B , Duncan J. Limpus B and Dean R. Jerry A CA School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4810, Australia.
B Aquatic Threatened Species Unit, Department of Environment and Heritage Protection, Brisbane, Qld 4001, Australia.
C Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Qld 4810, Australia.
D Corresponding author. Email: ericavtodd@gmail.com
Australian Journal of Zoology 60(6) 412-418 https://doi.org/10.1071/ZO13009
Submitted: 16 January 2013 Accepted: 6 May 2013 Published: 23 May 2013
Abstract
Genetic parentage studies can provide detailed insights into the mating system dynamics of wild populations, including the prevalence and patterns of multiple paternity. Multiple paternity is assumed to be common among turtles, though its prevalence varies widely between species and populations. Several important groups remain to be investigated, including the family Chelidae, which dominate the freshwater turtle fauna of the Southern Hemisphere. We used seven polymorphic microsatellite markers to investigate the presence of multiple fathers within clutches from the white-throated snapping turtle (Elseya albagula), an Australian species of conservation concern. We uncovered a high incidence of multiple paternity, with 83% of clutches showing evidence of multiple fathers and up to three males contributing to single clutches. We confirm a largely promiscuous mating system for this species in the Burnett River, Queensland, although a lone incidence of single paternity indicates it is not the only strategy employed. These data provide the first example of multiple paternity in the Chelidae and extend our knowledge of the taxonomic breadth of multiple paternity in turtles of the Southern Hemisphere.
Additional keywords: Burnett River, freshwater turtle, mating system, paternity assignment, polyandry.
References
Baer, B., and Schmid-Hempel, P. (1999). Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397, 151–154.| Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVyhtQ%3D%3D&md5=ba5b00ddfec4dcc167d69dcf7ac678aaCAS |
Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B. Methodological 57, 289–300.
Buhlmann, K. A., Akre, T. S. B., Iverson, J. B., Karapatakis, D., Mittermeier, R. A., Georges, A., Rhodin, A. G. J., van Dijk, P. P., and Gibbons, J. W. (2009). A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelonian Conservation and Biology 8, 116–149.
| A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas.Crossref | GoogleScholarGoogle Scholar |
Coleman, S. W., and Jones, A. G. (2011). Patterns of multiple paternity and maternity in fishes. Biological Journal of the Linnean Society. Linnean Society of London 103, 735–760.
| Patterns of multiple paternity and maternity in fishes.Crossref | GoogleScholarGoogle Scholar |
Davy, C. M., Edwards, T., Lathrop, A., Bratton, M., Hagan, M., Henen, B., Nagy, K. A., Stone, J., Hillard, L. S., and Murphy, R. W. (2011). Polyandry and multiple paternities in the threatened Agassiz’s desert tortoise, Gopherus agassizii. Conservation Genetics 12, 1313–1322.
| Polyandry and multiple paternities in the threatened Agassiz’s desert tortoise, Gopherus agassizii.Crossref | GoogleScholarGoogle Scholar |
Emlen, S. T., and Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223.
| Ecology, sexual selection, and the evolution of mating systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3hsFyrtQ%3D%3D&md5=1d06483d35f8fb79b8db49de4e7ddd6eCAS | 327542PubMed |
FitzSimmons, N. N. (1998). Single paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas). Molecular Ecology 7, 575–584.
| Single paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3ps1OmtQ%3D%3D&md5=557be5e9e73fee189b00bc16b7db477bCAS | 9633101PubMed |
Fleischer, R. C. (1996). Application of molecular methods to the assessment of genetic mating systems in vertebrates. In ‘Molecular Zoology: Advances, Strategies, and Protocols’. (Eds J. D. Ferris and S. R. Palumbi.) pp. 133–161. (John Wiley and Sons: New York.)
Galbraith, D. A. (1993). Multiple paternity and sperm storage in turtles. The Herpetological Journal 3, 117–123.
Garant, D., Dodson, J. J., and Bernatchez, L. (2001). A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.). The Journal of Heredity 92, 137–145.
| A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fht1Wktw%3D%3D&md5=78af526285eda196caefd9a084954f60CAS | 11396571PubMed |
Gist, D. H., and Jones, J. M. (1987). Storage of sperm in the reptilian oviduct. Scanning Microscopy 1, 1839–1849.
| 1:STN:280:DyaL1c7islSjsQ%3D%3D&md5=d062b3b94a9a3ad0931f3810eed444b2CAS | 3433065PubMed |
Gist, D. H., and Jones, J. M. (1989). Sperm storage within the oviduct of turtles. Journal of Morphology 199, 379–384.
| Sperm storage within the oviduct of turtles.Crossref | GoogleScholarGoogle Scholar |
Hamann, M., Schauble, C. S., Limpus, D. J., Emerick, S. P., and Limpus, C. J. (2007). Management plan for the conservation of Elseya sp. [Burnett River] in the Burnett River Catchment, Queensland, Australia. Queensland Environmental Protection Agency: Brisbane.
Harry, J. L., and Briscoe, D. A. (1988). Multiple paternity in the loggerhead turtle (Caretta caretta). The Journal of Heredity 79, 96–99.
| 1:STN:280:DyaL1c3pvFGrug%3D%3D&md5=e7723bbb269d14a7f1f7dc33769e02a9CAS | 3403964PubMed |
Hughes, C. (1998). Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology 79, 383–399.
| Integrating molecular techniques with field methods in studies of social behavior: a revolution results.Crossref | GoogleScholarGoogle Scholar |
Jensen, M. P., Abreu-Grobois, F. A., Frydenberg, J., and Loeschcke, V. (2006). Microsatellites provide insight into contrasting mating patterns in arribada vs. non-arribada Olive Ridley sea turtle rookeries. Molecular Ecology 15, 2567–2575.
| Microsatellites provide insight into contrasting mating patterns in arribada vs. non-arribada Olive Ridley sea turtle rookeries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVegt78%3D&md5=5edea71dd36048e541297dc08a125277CAS | 16842427PubMed |
Jones, A. G. (2005). GERUD 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Molecular Ecology Notes 5, 708–711.
| GERUD 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOhurrF&md5=3a167bb555d679798bd460ebac23adbaCAS |
Jones, A. G., and Ardren, W. R. (2003). Methods of parentage analysis in natural populations. Molecular Ecology 12, 2511–2523.
| Methods of parentage analysis in natural populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1Kqtbg%3D&md5=20a71a15f33ec77b2b8bd1f1fabf3c46CAS | 12969458PubMed |
Jones, O. R., and Wang, J. L. (2010). COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10, 551–555.
| COLONY: a program for parentage and sibship inference from multilocus genotype data.Crossref | GoogleScholarGoogle Scholar | 21565056PubMed |
Kalinowski, S. T., Taper, M. L., and Marshall, T. C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16, 1099–1106.
| Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment.Crossref | GoogleScholarGoogle Scholar | 17305863PubMed |
Karl, S. A. (2008). The effect of multiple paternity on the genetically effective size of a population. Molecular Ecology 17, 3973–3977.
| 19238700PubMed |
Lee, P. L. M., and Hays, G. C. (2004). Polyandry in a marine turtle: females make the best of a bad job. Proceedings of the National Academy of Sciences of the United States of America 101, 6530–6535.
| Polyandry in a marine turtle: females make the best of a bad job.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVyitbk%3D&md5=1f74387d12a6201e8a2bfa0d23820f85CAS |
Limpus, C. J., Limpus, D. J., Parmenter, C. J., Hodge, J., Forrest, M. J., and McLachlan, J. (2011). The biology and management strategies for freshwater turtles in the Fitzroy River Catchment, with particular emphasis on Elseya albagula and Rheodytes leukops. A study initiated in response to the proposed construction of Rookwood Weir and the raising of Eden Bann Weir. Department of Environment and Heritage Protection, Brisbane.
Lotterhos, K. E. (2011). The context-dependent effect of multiple paternity on effective population size. Evolution 65, 1693–1706.
| 21644957PubMed |
McTaggart, S. J. (2000). Good genes or sexy sons? Testing the benefits of female mate choice in the painted turtle, Chrysemys picta. Masters Thesis, University of Guelph, Canada.
Murphy, J. B., and Lamoreaux, W. E. (1978). Mating behavior in three Australian chelid turtles (Testudines: Pleurodira: Chelidae) Herpetologica 34, 398–405.
Murray, J. (1964). Multiple mating and effective population size in Cepaea nemoralis. Evolution 18, 283–291.
| Multiple mating and effective population size in Cepaea nemoralis.Crossref | GoogleScholarGoogle Scholar |
Neff, B. D., and Pitcher, T. E. (2002). Assessing the statistical power of genetic analyses to detect multiple mating in fishes. Journal of Fish Biology 61, 739–750.
| Assessing the statistical power of genetic analyses to detect multiple mating in fishes.Crossref | GoogleScholarGoogle Scholar |
Nunney, L. (1993). The influence of mating system and overlapping generations on effective population size. Evolution 47, 1329–1341.
| The influence of mating system and overlapping generations on effective population size.Crossref | GoogleScholarGoogle Scholar |
Pääbo, S., Poinar, H., Serre, D., Jaenicke-Despres, V., Hebler, J., Rohland, N., Kuch, M., Krause, J., Vigilant, L., and Hofreiter, M. (2004). Genetic analyses from ancient DNA. Annual Review of Genetics 38, 645–679.
| Genetic analyses from ancient DNA.Crossref | GoogleScholarGoogle Scholar | 15568989PubMed |
Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Pearse, D. E., and Anderson, E. C. (2009). Multiple paternity increases effective population size. Molecular Ecology 18, 3124–3127.
| Multiple paternity increases effective population size.Crossref | GoogleScholarGoogle Scholar | 19555411PubMed |
Pearse, D. E., and Avise, J. C. (2001). Turtle mating systems: behavior, sperm storage, and genetic paternity. The Journal of Heredity 92, 206–211.
| Turtle mating systems: behavior, sperm storage, and genetic paternity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fht1Wrtg%3D%3D&md5=7516b45414aa811b5fa71de013f354f7CAS | 11396580PubMed |
Pearse, D. E., Janzen, F. J., and Avise, J. C. (2002). Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behavioral Ecology and Sociobiology 51, 164–171.
| Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature.Crossref | GoogleScholarGoogle Scholar |
Reynolds, J. D. (1996). Animal breeding systems. Trends in Ecology & Evolution 11, 68–72.
| Animal breeding systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFerug%3D%3D&md5=6cc0e37220999bf72bf1ae8a9eec993aCAS |
Roques, S., Diaz-Paniagua, C., and Andreu, A. C. (2004). Microsatellite markers reveal multiple paternity and sperm storage in the Mediterranean spurthighed tortoise, Testudo graeca. Canadian Journal of Zoology 82, 153–159.
| Microsatellite markers reveal multiple paternity and sperm storage in the Mediterranean spurthighed tortoise, Testudo graeca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktFWhur0%3D&md5=38d9a86fddc8d078f2e1552ed605d624CAS |
Roques, S., Diaz-Paniagua, C., Portheault, A., Perez-Santigosa, N., and Hidalgo-Vila, J. (2006). Sperm storage and low incidence of multiple paternity in the European pond turtle, Emys orbicularis: a secure but costly strategy? Biological Conservation 129, 236–243.
| Sperm storage and low incidence of multiple paternity in the European pond turtle, Emys orbicularis: a secure but costly strategy?Crossref | GoogleScholarGoogle Scholar |
Rousset, F. (2008). Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
| Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar | 21585727PubMed |
Sever, D. M., and Hamlett, W. C. (2002). Female sperm storage in reptiles. The Journal of Experimental Zoology 292, 187–199.
| Female sperm storage in reptiles.Crossref | GoogleScholarGoogle Scholar | 11754034PubMed |
Stein, J. L., Stein, J. A., and Nix, H. A. (2002). Spatial analysis of anthropogenic river disturbance at regional and continental scales: identifying the wild rivers of Australia. Landscape and Urban Planning 60, 1–25.
| Spatial analysis of anthropogenic river disturbance at regional and continental scales: identifying the wild rivers of Australia.Crossref | GoogleScholarGoogle Scholar |
Sugg, D. W., and Chesser, R. K. (1994). Effective population sizes with multiple paternity. Genetics 137, 1147–1155.
| 1:STN:280:DyaK2M%2FntlKjsw%3D%3D&md5=a5ba9783049b9355d71b8b5e67f80c90CAS | 7982568PubMed |
Thomson, S., Georges, A., and Limpus, C. J. (2006). A new species of freshwater turtle in the genus Elseya (Testudines: Chelidae) from central coastal Queensland, Australia. Chelonian Conservation and Biology 5, 74–86.
| A new species of freshwater turtle in the genus Elseya (Testudines: Chelidae) from central coastal Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Todd, E., Blair, D., Hamann, M., and Jerry, D. (2011). Twenty-nine microsatellite markers for two Australian freshwater turtles, Elseya albagula and Emydura macquarii krefftii: development from 454-sequence data and utility in related taxa. Conservation Genetics Resources 3, 449–456.
| Twenty-nine microsatellite markers for two Australian freshwater turtles, Elseya albagula and Emydura macquarii krefftii: development from 454-sequence data and utility in related taxa.Crossref | GoogleScholarGoogle Scholar |
Todd, E. V., Blair, D., Farley, S., Farrington, L., FitzSimmons, N. N., Georges, A., Limpus, C. J., and Jerry, D. R. (). Contemporary genetic structure reflects historical drainage isolation in an Australian snapping turtle, Elseya albagula. Zoological Journal of the Linnean Society , .
Uller, T., and Olsson, M. (2008). Multiple paternity in reptiles: patterns and processes. Molecular Ecology 17, 2566–2580.
| Multiple paternity in reptiles: patterns and processes.Crossref | GoogleScholarGoogle Scholar | 18452517PubMed |
van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
| MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=8f159c0b84827ce791b15209338a9746CAS |
Wang, J. L. (2004). Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979.
| Sibship reconstruction from genetic data with typing errors.Crossref | GoogleScholarGoogle Scholar |
Wang, J. L., and Santure, A. (2009). Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181, 1579–1594.
| Parentage and sibship inference from multilocus genotype data under polygamy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFWqurk%3D&md5=c58a5ca90864c20319250cae3aaf7f07CAS |
Zbinden, J. A., Largiader, A. R., Leippert, F., Margaritoulis, D., and Arlettaz, R. (2007). High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Molecular Ecology 16, 3703–3711.
| High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtV2mu7%2FL&md5=249e93fb9e6c383062dfd6923613048fCAS | 17845442PubMed |