Hui WANG,Zhenhua LUO,Jian CHEN,et al.Social Polyandry and Multiple Paternity in the Omei Treefrog in the Southwest China[J].Asian Herpetological Research(AHR),2017,8(1):48-54.[doi:10.16373/j.cnki.ahr.160021]
Click Copy

Social Polyandry and Multiple Paternity in the Omei Treefrog in the Southwest China
Share To:

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2017 VoI.8 No.1
Research Field:
Publishing date:


Social Polyandry and Multiple Paternity in the Omei Treefrog in the Southwest China
Hui WANG# Zhenhua LUO# Jian CHEN Mian ZHAO and Hua WU*
Institute of Evolution and Ecology, School of Life Sciences, Central China Normal University, 152 Luoyulu, Hongshan District, Wuhan 430079, China.
Genetic polyandry multiple paternity Rhacophorus omeimontis social polyandry
Group spawning, polyandry reproductive behaviors, and multiple paternity are increasingly reported in anuran species. The Omei treefrog (Rhacophorus omeimontis), endemic to subtropical and mountainous forests of central and southwestern China, is a polyandrous lek-patterned breeder commonly showing multiple males-one female matings during the breeding season. To detect the traits of social and genetic polyandry in this species and explore the relationships between these traits, we investigated the breeding behaviors of a population of R. omeimontis in the Fengtongzhai National Nature Reserve, Baoxing County, Sichuan, China. We conducted paternity analyses using six microsatellite genetic markers. A total of 30 matings were recorded in the field (four monogamous pairs and 26 spawning groups). Our results revealed high proportions of social polyandry (86.7%) and multiple paternity (70.0%) and the numbers of joining males and genetic fathers among matings ranged from 1 to 8 and from 1 to 4, respectively. There was a significantly positive correlation between the intensities of social and genetic polyandry, indicating that multiple males-one female breeding behaviors could be an important promoter of multiple paternity. We considered the intense social polyandry and multiple paternity as consequences of intense male-male competition under a male-biased sex ratio and genetic benefits pursuing of the females. However, the proportion of genetic fathers in a spawning decreased with the increase of joining male number and most of their offspring belonged to a few males. This might be caused by a “making the best of a bad lot” reproductive strategy of the inferior male individuals.


Arnqvist G., Nilsson T. 2000. The evolution of polyandry: Multiple mating and female fitness in insects. Anim Behav, 60: 145–164
Awata S., Munehara H., Kohda M. 2005. Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: Field observations and parentage analyses. Behav Ecol Sociobiol, 58: 506–516
Bennett P. M., Owens I. P. F. 2002. Evolutionary ecology of birds life histories, mating systems and extinction, 1st Ed. Oxford: Oxford University Press
Brante A., Fernández M., Viard F. 2010. Microsatellite evidence for sperm storage and multiple paternity in the marine gastropod Crepidula coquimbensis. J Exp Mar Bio Ecol, 396: 83–88
Byrne P. G., Keogh J. S. 2009. Extreme sequential polyandry insures against nest failure in a frog. Proc R Soc B, 276: 115–120
Byrne P. G., Roberts J. D. 1999. Simultaneous mating with multiple males reduces fertilization success in the myobatrachid frog Crinia georgiana. Proc R Soc B, 266: 717–721
Byrne P. G., Roberts J. D. 2004. Intrasexual selection and group spawning in quacking frogs (Crinia georgiana). Behav Ecol, 15: 872–882
Byrne P. G., Whiting M. J. 2008. Simultaneous polyandry increases fertilization success in an African foam-nesting treefrog. Anim Behav, 76: 1157–1164
Byrne P. G., Whiting M. J. 2011. Effects of simultaneous polyandry on offspring fitness in an African tree frog. Behav Ecol, 22: 385–381
Caspers B. A., Krause E. T., Hendrix R., Kopp M., Rupp O., Rosentreter K., Steinfartz S. 2014. The more the better-polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra). Mol Ecol, 23: 239–250
Coleman S. W., Jones A. G. 2011. Patterns of multiple paternity and maternity in fishes. Biol J Linn Soc, 103: 735–760
Davies N. B., Halliday T. R. 1977. Optimal mate selection in the toad Bufo bufo. Nature, 269: 56–58
D’Orgeix C. A., Turner B. J. 1995. Multiple paternity in the red-eyed treefrog Agalychnis callidryas (Cope). Mol Ecol, 4: 505–508
Eberle M., Kappeler P. M. 2004. Selected polyandry: Female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behav Ecol Sociobiol, 57: 91–100
Eizaguirre C., Laloi D., Massot M., Richard M., Federici P., Clobert J. 2007. Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard. Proc R Soc B, 274: 425–430
Emlen S. T., Wrege P. H., Webster M. S. 1998. Cuckoldry as a cost of polyandry in the sex-role-reversed wattled jacana, Jacana jacana. Proc R Soc B, 265: 2359–2364
Evans J. P., Marshall D. J. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution, 59: 106–112
Fedorka K. M., Mousseau T. A. 2002. Material and genetic benefits of female multiple mating and polyandry. Anim Behav, 64: 361–367.
Fei L., Ye C. 2001. The colour handbook of amphibians of Sichuan. Beijing: China Forestry Publishing House
Fei L., Ye C., Jiang J. 2012. Colored atlas of Chinese amphibians and their distributions. Chengdu, China: Sichuan Science and Technology Press
Field D., Wills C. 1996. Long, polymorphic microsatellites in simple organisms. Proc R Soc B, 263: 209–215
Fisher R. A. 1915. The evolution of sexual preference. Eugen Rev, 7: 184–192
Fukuyama K. 1991. Spawning behaviour and male mating tactics of a foam-nesting treefrog, Rhacophorus schlegelii. Anim Behav, 42: 193–199
Gibson R. M., Jewell P. A. 1982. Semen quality, female choice and multiple mating in domestic sheep: A test of Trivers’ sexual competence hypothesis. Behaviour, 80: 9–31
Goudet J. 2002. Fstat v. Lausanne, Switzerland. Available at: (Accessed: 20 November 2015)
Halliday T. R., Tejedo M. 1995. Intrasexual selection and alternative mating behaviour. 419–468. In Heatwole H., Sullivan B. K. (Eds.), Amphibian Biology, Vol. 2, Social Behaviour. Sydney: Surrey Beatty
Hancock J. M. 1996. Simple sequences in a ‘minimal’ genome. Nat Genet, 14: 14–15
Hosken D. J., Stockley P. 2003. Benefits of polyandry: A life history perspective. Evol Biol, 33: 173–194
Hurst G. D. D., Sharpe R. G., Broomfield A. H., Walker L. E., Majerus T. M. O., Zakharov I. A., Majerus M. E. N. 1995. Sexually transmitted disease in a polyandrous insect, Adalia bipunctata. Ecol Entomol, 20: 230–236
Jennions M. D., Blackwell P. R. Y., Passemore N. I. 1992. Breeding behaviour of the African frog, Chiromantis xerampelina: Multiple spawning and polyandry. Anim Behav, 44: 1091–1100
Kalinowski S. T., Taper M. L., Marshall T. C. 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol, 16: 1099–1106
Klemme I., Yl?nen H., Eccard J. A. 2008. Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus. Proc R Soc B, 275: 1095–1100
Laurila A., Sepp? P. 1998. Multiple paternity in the common frog (Rana temporaria): Genetic evidence from tadpole kin groups. Biol J Linn Soc, 63: 221–232
Lesobre L., Lacroix F., Le Nuz E., Hingrat Y., Chalah T., Jaime M. S. 2010. Absence of male reproductive skew, along with high frequency of polyandry and conspecific brood parasitism in the lekking Houbara bustard Chlamydotis undulata undulata. J Avian Biol, 41: 117–127
Levitan D. R. 1998. Sperm limitation, gamete competition, and sexual selection in external fertilizers. 173–215. In Birkhead T. R., M?ller A. P. (Eds.). Sperm Competition and Sexual Selection. San Diego, USA: Academic Press
Liao W., Lu X. 2010. Breeding behavior of the Omei treefrog Rhacophorus omeimontis (Anura: Rachophoridae) in a subtropical montane region. J Nat Hist, 44: 2929–2940
Liao W., Lu X. 2011. Male mating success in the Omei treefrog (Rhacophorus omeimontis): The influence of body size and age. Belg J Zool, 141: 3–10
Lodé T., Lesbarrères D. 2004. Multiple paternity in Rana dalmatina, a monogamous territorial breeding anuran. Naturwissenschaften, 91: 44–47
Luo Z., Hu M., Hong M., Li C., Gu Q., Gu Z., Liao C., Zhao M., Wu H. 2015. Outbreeding avoidance as probable driver of mate choice in the Asiatic toad. J Zool, 295: 223–231
Luo Z., Li C., Wang H., Shen H., Zhao M., Gu Q., Liao C., Gu Z., Wu H. 2016. Male-male competition drives sexual selection and group spawning in the Omei treefrog, Rhacophorus omeimontis. Behav Ecol Sociobiol, 70: 593–605
Luo Z., Li C., Wang H., Zhao M., Gu Q., Gu Z., Liao C., Wu H. 2014. Mutual mate choice in the Asiatic toad, Bufo gargarizans, exerts stabilizing selection on body size. Chinese Sci Bull, 59: 38–45
Marshall T. C., Slate J., Kruuk L. E. B., Pemberton J. M. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol, 7: 639–655
Neff B. D., Pitcher T. E. 2005. Genetic quality and sexual selection: An integrated framework for good genes and compatible genes. Mol Ecol, 14: 19–38
Qi Y., Zhang W., Huang L., Luo Z., Zhao M., Wu H. 2015. Significant male biased sexual size dimorphism in Leptobrachium leishanensis. Asian Herpetol Res, 6: 169–175
Raymond M., Rousset F. 1995. Genepop (V1.3)-Population genetics software for exact tests and ecumenicism. J Hered, 86: 248–249
Rice W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature, 381: 232–234
Rice W. R., Stewart A. D., Morrow E. H., Linder J. E., Orteiza N., Byrne P. G. 2006. Assessing sexual conflict in the Drosophila melanogaster laboratory model system. Phil Trans R Soc B, 361: 287–299
Roberts D., Standish R. J., Byrne P. G., Doughty P. 1999. Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae). Anim Behav, 57: 721–726
Roberts J. D., Byrne P. G. 2011. Polyandry, sperm competition, and the evolution of anuran amphibians. Adv Stud Behav, 43: 1–53
Ronkainen K., Kaitala A., Kivel? S. M. 2010. Polyandry, multiple mating, and female fitness in a water strider Aquarius paludum. Behav Ecol Sociobiol, 64: 657–664
Rousset F. 2008. Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res, 8: 103–106
Rowe L. 1992. Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Anim Behav, 44: 189–202
Thornhill R., Alcock J. 1983. The evolution of insect mating systems. Cambridge: Harvard University Press
Tregenza T., Wedell N. 2002, Polyandrous females avoid costs of inbreeding. Nature, 415: 71–73
Wang C., Lu X. 2011. Female ground tits prefer relatives as extra-pair partners: Driven by kin-selection? Mol Ecol, 20: 2851–2863
Weber J. L., May P. E. 1989. Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am J Hum Genet, 44: 388–396
Yasui Y. 1998. The genetic benefits of female multiple mating reconsidered. Trends Ecol Evol, 13: 246–250
Yund P. O., McCartney M. A. 1994. Male reproductive success in sessile invertebrates: Competition for fertilizations. Ecology, 75: 2151–2167
Zeh J. A. 1997. Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion. Behav Ecol Sociobiol, 40: 111–118
Zhao M., Li C., Zhang W., Wang H., Luo Z., Gu Q., Gu Z., Liao C., Wu H. 2016. Male pursuit of higher reproductive success drives female polyandry in the Omei treefrog. Anim Behav, 111: 101–110
Zhao M., Zhang R., Li C., Mu T., Wei S., Li X., Wu H. 2012. Development of novel microsatellite markers in the Omei treefrog (Rhacophorus omeimontis). Int J Mol Sci, 13: 552–557


Last Update: 2017-03-25