Evolutionary Biology

, Volume 36, Issue 2, pp 201–213 | Cite as

Reproductive Success and Sexual Selection in Wild Eastern Tiger Salamanders (Ambystoma t. tigrinum)

Research Article

Abstract

Variation in reproductive success is most pronounced in species with strongly biased operational sex ratios, prominent sexual dimorphisms, and where mate competition and choice are likely. We studied sexual selection in eastern tiger salamanders (Ambystoma t. tigrinum) and examined the role of body size on reproductive success. We genotyped 155 adults and 1,341 larvae from 90 egg masses at six microsatellite loci. Parentage analyses revealed both sexes engaged in multiple matings, but was more common among females (64%) than males (27%). However, the standardized variance in mating and reproductive success was higher in males. Bateman gradients were significant and nearly identical in both sexes, suggesting that sexual selection was roughly equal between sexes. Body size was not correlated with mating or reproductive success in either sex. The apparent lack of sexual selection on body size may be a result of sperm storage, sperm competition, alternative mating tactics, and/or random induction of spermatophores.

Keywords

Bateman gradient Body size Mating success Microsatellites Parentage analysis Polygynandry 

Notes

Acknowledgements

We thank S. Baker, L. Sheets, S. Hecht, and numerous other technicians for help in collecting salamanders. We also thank members of the DeWoody lab for helpful comments on earlier drafts of this manuscript. Animals were collected under permits issued by the Indiana Department of Natural Resources and the Purdue University animal care and use committee. Financial support was provided by Purdue University and the National Science Foundation (DEB-0514815 awarded to J.A.D.). This is Agricultural Research Programs contribution number 2007-18264 from Purdue University.

References

  1. Andersson, M. (1982). Female choice selects for extreme tail length in a widowbird. Nature, 299, 818–820. doi: 10.1038/299818a0.CrossRefGoogle Scholar
  2. Arnold, S. J. (1976). Sexual behavior, sexual interference, and sexual defense in the salamanders Ambystoma maculatum, Ambystoma tigrinum, and Plethodon jordani. Zeitschrift fur Tierpsychologie, 42, 247–300.Google Scholar
  3. Arnold, S. J., & Duvall, D. (1994). Animal mating systems—A synthesis based on selection theory. American Naturalist, 143, 317–348. doi: 10.1086/285606.CrossRefGoogle Scholar
  4. Bateman, A. J. (1948). Intrasexual selection in Drosophila. Heredity, 2, 349–368. doi: 10.1038/hdy.1948.21.PubMedCrossRefGoogle Scholar
  5. Boisseau, C., & Joly, J. (1975). Transport and survival of spermatozoa in female Amphibia. In E. S. E. Hafez & C. G. Thibault (Eds.), The biology of spermatozoa (pp. 94–104). Karger, Switzerland: Basel.Google Scholar
  6. Bos, D. H., Williams, R. N., Gopurenko, D., Bulut, Z., & DeWoody, J. A. (2009). Condition dependent mate choice and a reproductive advantage for MHC-divergent male tiger salamanders. Molecular Ecology (in press).Google Scholar
  7. Brunton, D. H., Evans, B., Cope, T., & Ji, W. (2008). A test of the dear enemy hypothesis in female New Zealand bellbirds (Anthornis melanura): Female neighbors as threats. Behavioral Ecology, 19, 791–798. doi: 10.1093/beheco/arn027.CrossRefGoogle Scholar
  8. Chandler, C. H., & Zamudio, K. R. (2008). Reproductive success by large, closely related males facilitated by sperm storage in an aggregate breeding amphibian. Molecular Ecology, 17, 1564–1576. doi: 10.1111/j.1365-294X.2007.03614.x.PubMedCrossRefGoogle Scholar
  9. Clutton-Brock, T. H. (1988). Reproductive success. In T. H. Clutton-Brock (Ed.), Reproductive success (pp. 472–485). Chicago: University of Chicago Press.Google Scholar
  10. Clutton-Brock, T. H. (2007). Sexual selection in males and females. Science, 318, 1882–1885. doi: 10.1126/science.1133311.PubMedCrossRefGoogle Scholar
  11. DeWoody, J. A. (2005). Molecular approaches to the study of parentage, relatedness and fitness: Practical applications for wild animals. The Journal of Wildlife Management, 69, 1400–1418. doi: 10.2193/0022-541X(2005)69[1400:MATTSO]2.0.CO;2.CrossRefGoogle Scholar
  12. Douglas, M. E., & Monroe, B. L., Jr. (1981). A comparative study of topographical orientation in Ambystoma (Amphibia: Caudata). Copeia, 198, 460–463. doi: 10.2307/1444239.CrossRefGoogle Scholar
  13. Duchesne, P., Godbout, M. H., & Bernatchez, L. (2002). PAPA: A computer program for simulated and real parental allocation. Molecular Ecology Notes, 2, 191–194. doi: 10.1046/j.1471-8286.2002.00164.x.CrossRefGoogle Scholar
  14. Eberhard, W. G. (1996). Female control: Sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.Google Scholar
  15. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223. doi: 10.1126/science.327542.PubMedCrossRefGoogle Scholar
  16. Fedorka, K. M., & Mousseau, T. A. (2002). Material and genetic benefits of female multiple mating and polyandry. Animal Behaviour, 64, 361–367. doi: 10.1006/anbe.2002.3052.CrossRefGoogle Scholar
  17. Gabor, C. R., & Halliday, T. R. (1997). Sequential mate choice by smooth newts: Females become more choosy. Behavioral Ecology, 8, 162–166. doi: 10.1093/beheco/8.2.162.CrossRefGoogle Scholar
  18. Gabor, C. R., Krenz, J. D., & Jaeger, R. G. (2000). Female choice, male interference, and sperm precedence in the red-spotted newt. Behavioral Ecology, 11, 115–124. doi: 10.1093/beheco/11.1.115.CrossRefGoogle Scholar
  19. Gill, D. E. (1978). The metapopulation ecology of the red-spotted newt, Notophthalmus viridescens. Ecological Monographs, 48, 145–166. doi: 10.2307/2937297.CrossRefGoogle Scholar
  20. Gladstone, D. E. (1979). Promiscuity in monogamous colonial birds. American Naturalist, 114, 545–557. doi: 10.1086/283501.CrossRefGoogle Scholar
  21. Gopurenko, D., Williams, R. N., & DeWoody, J. A. (2007). Reproductive and mating success in the small-mouthed salamander (Ambystoma texanum) estimated via microsatellite parentage analysis. Evolutionary Biology, 34, 130–139. doi: 10.1007/s11692-007-9009-0.CrossRefGoogle Scholar
  22. Gopurenko, D., Williams, R. N., McCormick, C. R., & DeWoody, J. A. (2006). Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses. Molecular Ecology, 5, 1917–1928. doi: 10.1111/j.1365-294X.2006.02904.x.CrossRefGoogle Scholar
  23. Gowaty, P. A. (2004). Sex roles, contests for the control of reproduction, and sexual selection. In P. Kappeler & C. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 37–54). Cambridge, UK: Cambridge University Press.Google Scholar
  24. Gowaty, P. A., & Hubbell, S. P. (2005). Chance, time allocation, and the evolution of adaptively flexible sex role behavior. Integrative and Comparative Biology, 45, 931–944. doi: 10.1093/icb/45.5.931.CrossRefGoogle Scholar
  25. Halliday, T. R. (1983). The study of mate choice. In P. Bateson (Ed.), Mate choice. Cambridge: Cambridge University Press.Google Scholar
  26. Halliday, T. (1998). Sperm competition in amphibians. In T. R. Birkhead & A. P. Moller (Eds.), Sperm competition and sexual selection. SanDiego: Academic Press.Google Scholar
  27. Halliday, T., & Arnold, S. J. (1987). Multiple mating by females: A perspective from quantitative genetics. Animal Behaviour, 35, 939–941. doi: 10.1016/S0003-3472(87)80138-0.CrossRefGoogle Scholar
  28. Harris, W. E., & Lucas, J. R. (2002). A state-based model of sperm allocation in a group-breeding salamander. Behavioral Ecology, 13, 705–712. doi: 10.1093/beheco/13.5.705.CrossRefGoogle Scholar
  29. Houck, L. D. (1988). The effect of body size on male courtship success in a plethodontid salamander. Animal Behaviour, 36, 837–842. doi: 10.1016/S0003-3472(88)80166-0.CrossRefGoogle Scholar
  30. Houck, L. K., & Arnold, S. J. (2003). Courtship and mating behavior. In D. M. Sever (Ed.), Reproductive biology and phylogeny of Urodela (pp. 383–424). Enfield, NH: Science Publishers Inc.Google Scholar
  31. Houck, L. D., Tilley, S. G., & Arnold, S. J. (1985). Sperm competition in a plethodontid salamander: Preliminary results. Journal of Herpetology, 19, 420–423. doi: 10.2307/1564273.CrossRefGoogle Scholar
  32. Howard, R. D., Moorman, R. S., & Whiteman, H. H. (1997). Differential effects of mate competition and mate choice on eastern tiger salamanders. Animal Behaviour, 53, 1345–1356. doi: 10.1006/anbe.1996.0359.PubMedCrossRefGoogle Scholar
  33. Hubbell, S. P., & Johnson, S. K. (1987). Environmental variance in lifetime mating success, mate choice, and sexual selection. American Naturalist, 130, 91–112. doi: 10.1086/284700.CrossRefGoogle Scholar
  34. Humphrey, R. R. (1977). Factors influencing ovulation in the Mexican axolotyl as revealed by induced spawning. The Journal of Experimental Zoology, 199, 209–214. doi: 10.1002/jez.1401990205.PubMedCrossRefGoogle Scholar
  35. Janzen, F. J., & Brodie, E. D., III (1989). Tall tails and sexy males: Sexual behavior of rough-skinned newts (Taricha granulosa) in a natural breeding pond. Copeia, 1989, 1068–1071. doi: 10.2307/1446002.CrossRefGoogle Scholar
  36. Jones, A. G., Adams, E. M., & Arnold, S. J. (2002a). Topping off: A mechanism of first-mail sperm precedence in a vertebrate. Proceedings of the National Academy of Sciences of the United States of America, 99, 2078–2081. doi: 10.1073/pnas.042510199.PubMedCrossRefGoogle Scholar
  37. Jones, A. G., Arguello, J. R., & Arnold, S. J. (2002b). Validation of Bateman’s principles: A genetic study of sexual selection and mating patterns in the rough-skinned newt. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269, 2533–2539. doi: 10.1098/rspb.2002.2177.PubMedCrossRefGoogle Scholar
  38. Jones, A. G., Arguello, J. R., & Arnold, S. J. (2004). Molecular parentage analysis in experimental newt populations: The response of mating system measures to variation in the operational sex ratio. American Naturalist, 164, 444–456. doi: 10.1086/423826.PubMedCrossRefGoogle Scholar
  39. Jones, B., Grossman, G. D., Walsh, D. C. I., Porter, B. A., Avise, J. C., & Fiumera, A. C. (2007). Estimating differential reproductive success from nests of related individuals, with application to a study of the mottled sculpin, Cottus bairdi. Genetics, 176, 2427–2439. doi: 10.1534/genetics.106.067066.PubMedCrossRefGoogle Scholar
  40. Jones, A. G., Rosenqvist, G., Berglund, A., & Avise, J. C. (2005). The measurement of sexual selection using Bateman’s principles: An experimental test in the sex-role-reversed pipefish Syngnathus typhle. Integrative and Comparative Biology, 45, 874–884. doi: 10.1093/icb/45.5.874.CrossRefGoogle Scholar
  41. Ketterson, E. D., Parker, P. G., Raouf, S. A., Nolan, V., Ziegenfus, C., & Chandler, C. R. (1998). Bateman’s paradigm as a case study. In P. G. Parker & N. T. Burley (Eds.), Avian reproductive tactics: Female and male perspectives (pp. 81–101). Lawrence, KS: Allen Press.Google Scholar
  42. Kumpf, K. F. (1934). The courtship of Ambystoma tigrinum. Copeia, 1934, 7–10. doi: 10.2307/1436425.CrossRefGoogle Scholar
  43. Levitan, D. R. (1998). Sperm limitation, sperm competition and sexual selection in external fertilizers. In T. Birkhead & A. Moller (Eds.), Sperm competition and sexual selection (pp. 173–215). New York: Academic Press.Google Scholar
  44. Levitan, D. R. (2005). The distribution of male and female reproductive success in a broadcast spawning marine invertebrate. Integrative and Comparative Biology, 45, 848–855. doi: 10.1093/icb/45.5.848.CrossRefGoogle Scholar
  45. Lorch, P. D., Bussière, L., & Gwynne, D. T. (2008). Quantifying the potential for sexual dimorphism using upper limits on Bateman gradients. Behaviour, 145, 1–24.CrossRefGoogle Scholar
  46. Marshall, T. C., Slate, J., Kruuk, L. E. B., & Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7, 639–655. doi: 10.1046/j.1365-294x.1998.00374.x.PubMedCrossRefGoogle Scholar
  47. Mech, S. G., Storfer, A., Ernst, J. A., Reudink, M. W., & Maloney, S. D. (2003). Polymorphic microsatellite loci for tiger salamanders, Ambystoma tigrinum. Molecular Ecology Notes, 3, 79–81. doi: 10.1046/j.1471-8286.2003.00356.x.CrossRefGoogle Scholar
  48. Morrissey, M. B., & Wilson, A. J. (2005). The potential cost of accounting for genotypic errors in molecular parentage analysis. Molecular Ecology, 14, 4111–4121. doi: 10.1111/j.1365-294X.2005.02708.x.PubMedCrossRefGoogle Scholar
  49. Newcomer, S. D., Zeh, J. A., & Zeh, D. W. (1999). Genetic benefits enhance the reproductive success of polyandrous females. Proceedings of the National Academy of Sciences of the United States of America, 96, 10236–10241. doi: 10.1073/pnas.96.18.10236.PubMedCrossRefGoogle Scholar
  50. Olsson, M. (1993). Male preference for large females and assortative mating for body size in the sand lizard (Lacerta agilis). Behavioral Ecology and Sociobiology, 32, 337–341. doi: 10.1007/BF00183789.CrossRefGoogle Scholar
  51. Parra-Olea, G., Recuero, E., & Zamudio, K. R. (2007). Polymorphic microsatellite markers for Mexican salamanders of the genus Ambystoma. Molecular Ecology Notes, 7, 818–820. doi: 10.1111/j.1471-8286.2007.01714.x.CrossRefGoogle Scholar
  52. Peakall, R., & Smouse, P. E. (2006). Genalex 6: Genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295. doi: 10.1111/j.1471-8286.2005.01155.x.CrossRefGoogle Scholar
  53. Peckham, R. S., & Dineen, C. F. (1954). Spring migrations of salamanders. Proceedings of the Indiana Academy of Sciences, 64, 278–280.Google Scholar
  54. Petranka, J. A. (1998). Salamanders of the United States and Canada. Washington, DC: Smithsonian Institution.Google Scholar
  55. Phillips, C. A., & Sexton, O. J. (1989). Orientation and sexual differences during breeding migration of the spotted salamander, Ambystoma maculatum. Copeia, 1989, 17–22. doi: 10.2307/1445599.CrossRefGoogle Scholar
  56. Queller, D. C., & Goodnight, K. F. (1989). Estimating relatedness using genetic markers. Evolution, 43, 258–275.CrossRefGoogle Scholar
  57. Regosin, J. J. V., Windmiller, B. S., Homan, R. N., & Reed, J. M. (2005). Variation in terrestrial habitat use by four pool-breeding amphibian species. The Journal of Wildlife Management, 69, 1481–1493. doi: 10.2193/0022-541X(2005)69[1481:VITHUB]2.0.CO;2.CrossRefGoogle Scholar
  58. Rose, F. L., & Armentrout, D. (1976). Adaptive strategies of Ambystoma tigrinum (Green) inhabiting the Llano Estacado of west Texas. Journal of Animal Ecology, 45, 713–729. doi: 10.2307/3577.CrossRefGoogle Scholar
  59. Sambrook, J., & Russell, D. W. (2001). Molecular cloning: A laboratory manual (3rd ed.). Cold Springs Harbor, NY: Cold Springs Harbor Laboratory Press.Google Scholar
  60. Sarhan, A., & Kokko, H. (2007). Multiple mating in the Glanville fritillary butterfly: A case of within-generation bet-hedging? Evolution; International Journal of Organic Evolution, 61, 606–616. doi: 10.1111/j.1558-5646.2007.00053.x.PubMedGoogle Scholar
  61. Schulte-Hostedde, A. I., Millar, J. S., & Gibbs, H. L. (2004). Sexual selection and mating patters in a mammal with female-biased sexual size dimorphism. Behavioral Ecology, 15, 351–356. doi: 10.1093/beheco/arh021.CrossRefGoogle Scholar
  62. Semlitsch, R. D. (1998). Biological delineation of terrestrial buffer zones for pond breeding salamanders. Conservation Biology, 12, 1113–1119. doi: 10.1046/j.1523-1739.1998.97274.x.CrossRefGoogle Scholar
  63. Sever, D. M. (1995). Spermathecae of Ambystoma tigrinum (Amphibia: Caudata): Development and a role for the secretions. Journal of Herpetology, 29, 243–255. doi: 10.2307/1564561.CrossRefGoogle Scholar
  64. Sever, D. M. (2002). Female sperm storage in amphibians. The Journal of Experimental Zoology, 292, 165–179. doi: 10.1002/jez.1152.PubMedCrossRefGoogle Scholar
  65. Sever, D. M. (Ed.). (2003). Courtship and mating glands. In Reproductive biology and Phylogeny of Urodela. New Hampshire: Science Publishers, Inc.Google Scholar
  66. Sever, D. M., & Dineen, C. F. (1978). Reproductive ecology of the tiger salamander, Ambystoma tigrinum, in northern Indiana. Proceedings of the Indiana Academy of Sciences, 87, 189–203.CrossRefGoogle Scholar
  67. Sever, D. M., Rania, L. C., & Krenz, J. D. (1996). Annual cycle of sperm storage in spermathecae of the red-spotted newt, Notophthalmus viridescens (Amphbiia:Salamandridae). Journal of Morphology, 227, 155–170. doi: 10.1002/(SICI)1097-4687(199602)227:2<155::AID-JMOR3>3.0.CO;2-8.CrossRefGoogle Scholar
  68. Shillington, C., & Verrell, P. (1996). Multiple mating by females is not dependent on body size in the salamander Desmognathus ocrophaeus. Amphibia-Reptilia, 17, 33–38. doi: 10.1163/156853896X00261.CrossRefGoogle Scholar
  69. Shuster, S. M., & Wade, M. J. (2003). Mating systems and strategies. Princeton, NJ: Princeton University Press.Google Scholar
  70. Sinervo, B., & Zamudio, K. R. (2001). The evolution of alternative reproductive strategies: Fitness differential, heritability, and genetic correlation between the sexes. The Journal of Heredity, 92, 198–205. doi: 10.1093/jhered/92.2.198.PubMedCrossRefGoogle Scholar
  71. Skelly, D. K. (2002). Experimental venue and estimation of interaction strength. Ecology, 83, 2097–2101.Google Scholar
  72. Skelly, D. K. (2004). Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution; International Journal of Organic Evolution, 58, 160–165.PubMedGoogle Scholar
  73. Snyder, B. F., & Gowaty, P. A. (2007). A reappraisal of Bateman’s classic study of intrasexual selection. Evolution; International Journal of Organic Evolution, 61, 2457–2468. doi: 10.1111/j.1558-5646.2007.00212.x.PubMedGoogle Scholar
  74. Stearns, S. C. (1992). The evolution of life histories. Oxford, UK: Oxford University Press.Google Scholar
  75. Tang-Martinez, Z., & Ryder, T. B. (2005). The problem with paradigms: Bateman’s worldview as a case study. Integrative and Comparative Biology, 45, 821–830. doi: 10.1093/icb/45.5.821.CrossRefGoogle Scholar
  76. Tennessen, J. A., & Zamudio, K. R. (2003). Early male reproductive advantage, multiple paternity and sperm storage in an amphibian aggregate breeder. Molecular Ecology, 12, 1567–1576. doi: 10.1046/j.1365-294X.2003.01830.x.PubMedCrossRefGoogle Scholar
  77. Trauth, S. E., Sever, D. M., & Semlitsch, R. D. (1994). Cloacal anatomy of paedomorphic female Ambystoma talpoideum (Caudata: Ambystomatidae), with comments on intermorph mating and sperm storage. Canadian Journal of Zoology, 72, 2147–2157. doi: 10.1139/z94-287.CrossRefGoogle Scholar
  78. Twitty, V. C. (1966). Of scientists and salamanders. San Francisco, CA: Freeman.Google Scholar
  79. Verrell, P. A. (1984). Sexual interference and sexual defense in the smooth newt, Triturus vulgaris (Amphibia:Urodela: Salamandridae). Zeitschrift fur Tierpsychologie, 66, 242–254.Google Scholar
  80. Verrell, P. A. (1989a). Male mate choice for fecund females in a plethodontid salamander. Animal Behaviour, 38, 1086–1088. doi: 10.1016/S0003-3472(89)80150-2.CrossRefGoogle Scholar
  81. Verrell, P. A. (1989b). The sexual strategies of natural populations of newts and salamanders. Herpetology, 45, 265–281.Google Scholar
  82. Verrell, P. A. (1995). Males choose larger females as mates in the salamander Desmognathus santeelah. Ethology, 99, 162–171.CrossRefGoogle Scholar
  83. Verrell, P., Halliday, T., & Griffiths, M. (1986). The annual reproductive cycle of the smooth newt (Triturus vulgaris) in England. Journal of Zoology, 210, 101–119.Google Scholar
  84. Verrell, P., & McCabe, N. (1988). Field observations of the sexual behaviour of the smooth newt, Triturus vulgaris vulgaris (Amphibia: Salamandridae). Journal of Zoology, 214, 533–545.CrossRefGoogle Scholar
  85. Waser, P. M., & DeWoody, J. A. (2006). Multiple paternity in a philopatric rodent: The interaction of competition and choice. Behavioral Ecology, 17, 971–978. doi: 10.1093/beheco/arl034.CrossRefGoogle Scholar
  86. Williams, R. N., & DeWoody, J. A. (2004). Fluorescent dUTP helps characterize 10 novel tetranucleotide microsatellites from an enriched salamander (Ambystoma texanum) genomic library. Molecular Ecology Notes, 4, 17–19. doi: 10.1046/j.1471-8286.2003.00559.x.CrossRefGoogle Scholar
  87. Williams, R. N., Gopurenko, D., Kemp, K. R., Williams, B., & DeWoody, J. A. (2009). Breeding chronology, sexual dimorphism, and genetic diversity of congeneric ambystomatid salamanders. Journal of Herpetology (in press).Google Scholar
  88. Worden, B. D., & Parker, P. G. (2001). Polyandry in grain beetles leads to greater reproductive success: Material and genetic benefits? Behavioral Ecology, 12, 761–767. doi: 10.1093/beheco/12.6.761.CrossRefGoogle Scholar
  89. Zar, J. (1999). Biostatistical analysis (4th ed.). New Jersey: Prentice-Hall.Google Scholar
  90. Zeh, J. A., & Zeh, D. W. (2001). Reproductive mode and the genetic benefits of polyandry. Animal Behaviour, 61, 1051–1063. doi: 10.1006/anbe.2000.1705.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Forestry and Natural ResourcesPurdue UniversityWest LafayetteUSA

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