Abstract
Male tigers (Panthera tigris altaica) in captivity copulate alternatively with an estrous female, suggesting a potential for heteropaternity as an effective reproductive strategy to maximize genetic diversity of offspring. We analyzed microsatellites to test and compare the genetic output of multiple male mating (simultaneous polyandry) and single male mating (monogamy) with a female in a captive population. Simultaneous polyandry resulted in heteropaternity in 66.7% observed litters. No significant differences between parental populations and between offspring populations were detected in the number of alleles (A), expected heterozygosity (H e), number of effective alleles (N e) per locus and standard individual heterozygosity (SH) (P>0.05 for all 4 indexes). Comparisons showed no significant reduction of A, H o, H e and SH from parental population to offspring population for the two mating modes (P>0.05) except for SH in polyandrous families (P=0.029). However, such reduction was equivalent to single mating families when the influence of relatedness was eliminated using effective SH (E SH ) (P>0.05). These results highlight an alternative strategy for managing captive populations of tiger and other wild felids in which animals are combined at one location allowing for copulation by multiple males to encourage heteropaternity in favor of maintained genetic diversity among offspring.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Wilcken J, Lees C. Managing Zoo Populations: Compiling and Analysing Studbook Data. Mosman, Australia: Australasian Regional Association of Zoological Parks and Aquaria. Available from the Federation of Zoos, ZSL, London. 1998
Frankham R, Ballou J D, Briscoe D A. Introduction to Conservation Genetics. Cambridge: Cambridge University Press, 2002. 336–359
Tregenza T, Wedell N. Genetic compatibility, mate choice and patterns of parentage: Invited review. Mol Ecol, 2000, 9: 1013–1027
Crowell-Davis S L, Curtis T M, Knowles R J. Social organization in the cat: A modern understanding. J Feline Med Surg, 2004, 6: 19–28
Ishida Y, Yahara T, Kasuya E, et al. Female control of paternity during copulation: Inbreeding avoidance in feral cats. Behaviour, 2001, 138: 235–250
Say L, Pontier D, Natoli E. High variation in multiple paternity of domestic cats (Felis catus L.) in relation to environmental conditions. Proc Royal Soc B, 1999, 266: 2071–2074
James W H. The incidence of superfecundation and of double paternity in the general population. Acta Genet Med Gemallol (Roma), 1993, 42: 257–262
Bercovitch F B, Widdig A, Berard J D, et al. Multiple sirehood in free-ranging twin rhesus macaques (Macaca mulatta). Am J Primatol, 2002, 57: 31–34
Radespiel U, dal Secco V, Drögemüller C, et al. Sexual selection, multiple mating and paternity in grey mouse lemurs, Microcebus murinus. Anim Behav, 2002, 63: 259–268
Ely J J, Frels W I, Howell S, et al. Twinning and heteropaternity in chimpanzees (Pan troglodytes). Am J Phys Anthropol, 2006, 130: 96–102
Tregenza T, Wedell N. Polyandrous females avoid costs of inbreeding. Nature, 2002, 415: 71–73
Hanken J, Sherman P W. Multiple paternity in Belding’s ground squirrel litters. Science, 1981, 212: 351–353
Murie J O. Mating behavior of Columbian ground squirrels: I. Multiple mating by females and multiple paternity. Can J Zool, 1996, 73: 1819–1826
Sillero-Zubiri C, Gottelli D, Macdonald D W. Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav Ecol Sociobiol, 1996, 38: 331–340
Cordero P J. Extra-pair paternity in birds: ‘Good-genes’ and something else. Trends Ecol Evol, 1998, 13: 280
Foerster K, Delhey K, Johnsen A, et al. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature, 2003, 425: 714–717
Jennions M D, Petrie M. Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Phil Soc, 2000, 75: 21–64
Yasui Y. Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable. Ecol Res, 2001, 16: 605–616
Stockley P. Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc Royal Soc B, 2003, 270: 271–278
Wolff J O, Macdonald D W. Promiscuous females protect their offspring. Trends Ecol Evol, 2004, 19: 127–134
Mazák V. Panthera tigris. Mammal Sp, 1981, 152: 1–8
Smith J L D, McDougal C W, Sunquist M E. Female land tenure system in tigers. In: Tilson R L, Seal U S, eds. Tigers of the World: the Biology, Biopolitics, Management and Conservation of an Endangered Species. New Jersey: Noyes Publications, 1987. 97–109
Panwar H S. Project tiger: The reserves, the tigers, and their future. In: Tilson R L, Seal U S, eds. Tigers of the World: the Biology, Biopolitics, Management and Conservation of an Endangered Species. New Jersey: Noyes Publications, 1987. 110–117
Schaller G B. The Deer and the Tiger: A Study of Wildlife in India. Chicago: University of Chicago Press, 1967. 370
Bragin A P. Territorial behavior and possible mechanisms of regulation of the population density in the Amur tiger (Panther tigris altaica). Zool Zh, 1986, 65: 272–282
Butler J M, David V A, O’Brien S J, et al. The MeowPlex: A new DNA test using tetranucleotide STR markers for the domestic cat. Profiles in DNA, Promega Corp, 2002, 5: 7–10
David V A, Menotti-Raymond M. Automated DNA Detection with Fluorescent-based Technologies. Oxford: IRL Press, 1998
Yeh F C, Yang R C, Boyle T B J, et al. POPGENE version 1.32, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada. 2001. (http://www.ualberta.ca/~fyeh/download.htm)
DeNise S, Johnston E, Halverson J, et al. Power of exclusion for parentage verification and probability of match for identity in American kennel club breeds using 17 canine microsatellite markers. Anim Genet, 2003, 35: 14–17
Rousset F. Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resources, 2008, 8: 103–106
Jamieson A. The effectiveness of using codominant polymorpic allelic series for (1) checking pedigrees and (2) distinguishing fullsib pair members. Anim Genet, 1994, 25: 37–44
Coltman D W, Pilkington J G, Smith J A, et al. Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution, 1999, 53: 1259–1267
Kalinowski S T, Wagner A P, Taper M A L. ML-RELATE: A computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes, 2006, 6: 576–579
Gottelli D, Wang J L, Bashir S, et al. Genetic analysis reveals promiscuity among female cheetahs. Proc Royal Soc B, 2007, 274: 1993–2001
Brown J L. A theory of mate choice based on heterozygosity. Behav Ecol, 1997, 8: 60–65
Bensch S, Andrén H, Hansson B, et al. Selection for heterozygosity gives hope to a wild population of inbred wolves. PLoS One, 2006, 1: e72. doi: 0.1371/journal.pone.0000072
Clutton-Brock T H. Mammalian mating systems. Proc Royal Soc B, 1989, 236: 339–372
Birkhead T. Promiscuity. Cambridge: Harvard University Press, 2000
Xu Y C, Fang S G, Li Z K. Sustainability of the South China tiger: Implications of inbreeding depression and introgression. Conserv Genet, 2007, 8: 1199–1207
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contributed equally to this work.
This article is published with open access at Springerlink.com
Rights and permissions
This article is published under an open access license. Please check the 'Copyright Information' section either on this page or in the PDF for details of this license and what re-use is permitted. If your intended use exceeds what is permitted by the license or if you are unable to locate the licence and re-use information, please contact the Rights and Permissions team.
About this article
Cite this article
Liu, D., Ma, Y., Li, H. et al. Simultaneous polyandry and heteropaternity in tiger (Panthera tigris altaica): Implications for conservation of genetic diversity in captive populations of felids. Chin. Sci. Bull. 58, 2230–2236 (2013). https://doi.org/10.1007/s11434-013-5722-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11434-013-5722-5