Mating in a bisexually philopatric society: bottlenose dolphin females associate with adult males but not adult sons during estrous
- 309 Downloads
In fission-fusion societies, group size and composition change dynamically, reflecting social preferences and pressures. Most notably during reproduction, intersexual group dynamics reflect a balance between female choice for optimal mates and male competition for mating access. In systems where males and females remain in their natal area for life (bisexual philopatry), females can reduce the risk of incest by avoiding mating or associating with male kin. Shark Bay bottlenose dolphins (Tursiops aduncus) live in fission-fusion societies that enable them to exercise age, sex, and kin association biases. To determine how the balance between female choice and male competition is achieved, we examined adult female association with juvenile and adult males, including sons during female receptive periods, using 30 years of longitudinal data. Adult females demonstrated an increase in adult male association just prior to known conceptions, while juvenile male association consistently remained low. A decline in male association post-conception suggests that one or both sexes detect pregnancy early on. When we examined female association with juvenile and adult sons, a distinct pattern emerged. Adult females preferentially associated with sons compared to non-sons of the same age class post-weaning. Strikingly, females rarely associated with their adult sons when cycling. Our results suggest that (1) adult males either out-compete juvenile males in gaining access to fertile females or females prefer adult to juvenile males and (2) females mitigate the risk of close inbreeding by reducing association with sons when cycling.
No study has investigated behavioral strategies for reducing close inbreeding in bisexually philopatric, fluid mammal societies outside of humans. Using over 30 years of longitudinal data, we document how association dynamics change with female reproductive state. Post-weaning, mothers and sons associate, but almost never during conceptive periods. Adult male–female association is frequent during estrous, with a sharp decline after conception. Our study provides evidence for long-term kin recognition and detection of both estrous and early pregnancy among wild bottlenose dolphins. These findings have implications for the evolution of bisexual philopatry, fission-fusion dynamics, and infanticide—or lack thereof—in mammals.
KeywordsBisexual philopatry Estrous Inbreeding Juvenile Pregnancy Tursiops
We thank current and past members of the Shark Bay Dolphin Project, and numerous field assistants, for their efforts in data collection used for this project. In particular, we would like to acknowledge Ann-Marie Jacoby, Sara Eshleman, Jillian Wisse, Desirae Cambrelen, and Theodora Efthymiou. We are grateful to the Western Australia Department of Parks and Wildlife (DPaW) and the Monkey Mia Dolphin Resort for their logistical support in the field. We thank DPaW for contributing a portion of the life history data. We also thank two anonymous reviewers for their input on an earlier version of this manuscript. The study was funded by National Science Foundation grants 0941487, 0918308, 0316800, National Geographic Society Committee for Research and Exploration, ONR BAA 10230702, and Georgetown University.
Compliance with ethical standards
This work was approved by the Georgetown University Animal Care and Use Committee, permits #07–041, #10–023, #13-069, Western Australia Department of Parks and Wildlife permit #SF007418, #SF007975, #SF006897, #SF007457, #SF009311, #SF008076, #SF009876, and The University of Western Australia animal ethics permit #600-37. All procedures performed in this study were in accordance with the ethical standards of the aforementioned institutions and agencies. The study was funded by National Science Foundation grants 0941487, 0918308, 0316800, National Geographic Society Committee for Research and Exploration, ONR BAA 10230702, and Georgetown University.
Conflict of interest
The authors declare that they have no conflict of interest.
- Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics. Curr Anthropol 49:627–654Google Scholar
- Ayres KL, Booth RK, Hempelmann JA, Koski KL, Emmons CK, Baird RW, Balcomb-Bartok K, Hanson MB, Ford MJ, Wasser SK (2012) Distinguishing the impacts of inadequate prey and vessel traffic on an endangered killer whale (Orcinus orca) population. PLoS One 7:e36842CrossRefPubMedPubMedCentralGoogle Scholar
- Connor RC, Smolker RA, Richards AF (1992b) Dolphin alliances and coalitions. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, New York, pp 415–443Google Scholar
- Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin. Cetacean Societies, p 91–125Google Scholar
- Krzyszczyk E, Mann J (2012) Why become speckled? Ontogeny and function of speckling in Shark Bay bottlenose dolphins (Tursiops sp.)1. Mar Mamm Sci 28(2):295–307Google Scholar
- Mann J (2006) Establishing trust: socio-sexual behaviour and the development of male-male bonds among Indian Ocean bottlenose dolphins. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals: an evolutionary perspective. Cambridge University press, pp 107–130Google Scholar
- Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fenn 41:729–745Google Scholar
- Muggeo VM (2008) Segmented: an R package to fit regression models with broken-line relationships. R News 8:20–25Google Scholar
- Muraco HS (2015) Reproductive biology of the female bottlenose dolphin (Tursiops truncatus). Dissertation, Mississippi State UniversityGoogle Scholar
- O’Brien JK, Robeck TR (2012) The relationship of maternal characteristics and circulating progesterone concentrations with reproductive outcome in the bottlenose dolphin (Tursiops truncatus) after artificial insemination, with and without ovulation induction, and natural breeding. Theriogenology 78:469–482CrossRefPubMedGoogle Scholar
- Pagel MD, Harvey PH (2002) Evolution of the juvenile period in mammals. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. University of Chicago Press, Chicago, pp 28–37Google Scholar
- Pusey AE, Packer C (1987) Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate Societies. University of Chicago Press, Chicago, pp 250–266Google Scholar
- Robeck TR, Schneyer AL, McBain JF, Dalton LM, Walsh MT, Czekala NM, Kraemer DC (1993) Analysis of urinary immunoreactive steroid metabolites and gonadotropins for characterization of the estrous cycle, breeding period, and seasonal estrous activity of captive killer whales (Orcinus orca). Zoo Biol 12:173–187CrossRefGoogle Scholar
- Robeck TR, Steinman KJ, Yoshioka M, Jensen E, O’Brien JK, Katsumata E, Gili C, McBain JF, Sweeney J, Monfort SL (2005) Estrous cycle characterisation and artificial insemination using frozen–thawed spermatozoa in the bottlenose dolphin (Tursiops truncatus). Reproduction 129:659–674CrossRefPubMedGoogle Scholar
- van Schaik CP, Pradhan GR, van Noordwijk MA (2004) Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 131–150CrossRefGoogle Scholar
- Watson-Capps JJ (2005) Female mating behavior in the context of sexual coercion and female ranging behavior of bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Dissertation, Georgetown UniversityGoogle Scholar
- Wells RS (1991) The role of long-term study in understanding the social structure of a bottlenose dolphin community. In: Pryor K, Norris KS (eds) Dolphin societies: discoveries and puzzles. University of California Press, Berkeley, pp 199–225Google Scholar
- Wells RS (2014) Social structure and life history of common bottlenose dolphins near Sarasota Bay, Florida: insights from four decades and five generations. In: Yamigawa J, Karczmarski L (eds) Primates and cetaceans: field research and conservation of complex mammalian societies. Springer Press, Tokyo, pp 149–172CrossRefGoogle Scholar
- Wells RS, Scott MD (1990) Estimating bottlenose dolphin population parameters from individual identification and capture-release techniques. In: Hammond PS, Mizroch SA, Donovan GP (eds) Individual recognition of cetaceans: use of photo-identification and other techniques to estimate population parameters. Report of the international whaling commission, special issue 12, Cambridge, pp 407–415Google Scholar
- Wells RS, Scott MD, Irvine AB (1987) The social structure of free-ranging bottlenose dolphins. In: Genoways HH (ed) Current Mammalogy. Springer US, pp 247–305Google Scholar
- Whitehead H, Christal J, Tyack PL (2000) Studying cetacean social structure in space and time. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean Societies. University of Chicago Press, Chicago, pp 65–87Google Scholar
- Yuen WHQ (2007) An assessment of reproductive development of the male indo-Pacific bottlenose dolphin, Tursiops aduncus, in captivity. Dissertation, The Hong Kong Polytechnic UniversityGoogle Scholar