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Heterogeneous social associations within a sperm whale, Physeter macrocephalus, unit reflect pairwise relatedness

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Abstract

A good description of a social structure in which individuals live in stable social groups must also capture individual differences in social behaviour in order to understand the selective pressures behind formation and maintenance of those groups. Depending on the evolutionary mechanism acting and the nature of the benefits incurred by individuals, we might expect different patterns of intra-group associations. Female and immature sperm whales (Physeter macrocephalus, Linnaeus 1758) live in stable and partially matrilineal social units. Using photo identification and sloughed skin sampling for genetic determination of sex and relatedness, we investigated patterns of association within a social unit of sperm whales from the eastern Caribbean. Focus was given to how short-term spatio-temporal associations reflect relatedness among unit members. Contrary to previous findings, we found that the patterns of association among members of this unit were heterogeneous and that individuals had preferred associations or avoidances with specific individuals. Furthermore, these preferred associations correlate with relatedness between individuals, such that individuals associated more with their close relatives when variation in sociability of the individuals is controlled. These results are inconsistent with the simple equivalence model of homogeneous associations between members of a social unit. They indicate intra-unit social complexity, a basis for which seems to be genetic relatedness.

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References

  • Amos W, Whitehead H, Ferrari MJ, Glockner-Ferrari DA, Payne R, Gordon J (1992) Restrictable DNA from sloughed cetacean skin—its potential for use in population analysis. Mar Mamm Sci 8:275–283

    Article  Google Scholar 

  • Archie EA, Moss CJ, Alberts SC (2006) The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc R Soc Lond B 273:513–522

    Article  CAS  Google Scholar 

  • Arnbom T (1987) Individual identification of sperm whales. Rep Int Whal Comm 37:201–204

    Google Scholar 

  • Arnbom T, Papastavrou V, Weilgart LS, Whitehead H (1987) Sperm whales react to an attack by killer whales. J Mammal 68:450–453

    Article  Google Scholar 

  • Balcombe JP, Fenton MB (1988) Eavesdropping by bats: the influence of echolocation call design and foraging strategy. Ethology 79:158–166

    Article  Google Scholar 

  • Bejder L, Fletcher D, Bräger S (1998) A method of testing association patterns of social animals. Anim Behav 56:719–725

    Article  PubMed  Google Scholar 

  • Bérubé M, Palsbøll P (1996) Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol Ecol 5:283–287

    Article  PubMed  Google Scholar 

  • Best PB (1979) Social organization in sperm whales, Physeter macrocephalus. In: Winn HE, Olla BL (eds) Behaviour of marine animals: cetaceans. vol. 3. Plenum, New York, pp 227–289

    Google Scholar 

  • Best PB, Canham PAS, MacLeod N (1984) Patterns of reproduction in sperm whales, Physeter macrocephalus. Rep Int Whal Comm Spec Issue 6:51–79

    Google Scholar 

  • Buchanan FC, Friesen MK, Littlejohn RP, Clayton JW (1996) Microsatellites from the beluga whale Delphinapterus leucas. Mol Ecol 5:571–575

    Article  PubMed  CAS  Google Scholar 

  • Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469

    Article  Google Scholar 

  • Call J, Judge PG, De Wall FBM (1999) Influence of kinship and spatial density on reconciliation and grooming in rhesus monkeys. Am J Primatol 39:35–45

    Article  Google Scholar 

  • Christal J, Whitehead H (2001) Social affiliations within sperm whale (Physeter macrocephalus) groups. Ethology 107:323–340

    Article  Google Scholar 

  • Christal J, Whitehead H, Lettevall E (1998) Sperm whale social units: variation and change. Can J Zool 76:1431–1440

    Article  Google Scholar 

  • Clutton-Brock TH, Brotherton PNM, O’Riain MJ, Griffin AS, Gaynor D, Sharpe L, Kansky R, Manser MB, McIlrath GM (2000) Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta. Proc R Soc Lond B 267:301–305

    Article  CAS  Google Scholar 

  • Clutton-Brock TH, Brotherton PNM, O'Riain MJ, Griffin AS, Gaynor D, Kansky R, Sharpe L, McIlrath GM (2001) Contributions to cooperative rearing in meerkats. Anim Behav 61:705–710

    Article  Google Scholar 

  • Connor RC (1986) Pseudo-reciprocity—investing in mutualism. Anim Behav 34:1562–1566

    Article  Google Scholar 

  • Connor RC (1995) The benefits of mutualism—a conceptual-framework. Biol Rev Camb Philos Soc 70:427–457

    Article  Google Scholar 

  • Connor RC (2000) Group living in whales and dolphins. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, IL, pp 199–218

    Google Scholar 

  • Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission–fusion model. Proc R Soc Lond B 267:2213–2218

    Article  CAS  Google Scholar 

  • Durrell JL, Sneddon IA, O'Connell NE, Whitehead H (2004) Do pigs form preferential associations? Appl Anim Behav Sci 89:41–52

    Article  Google Scholar 

  • Ellard ME, Crowell-Davis SL (1989) Evaluating equine dominance in draft mares. Appl Anim Behav Sci 24:55–75

    Article  Google Scholar 

  • Engelhaupt D (2004) Phylogeography, kinship and molecular ecology of sperm whales (Physeter macrocephalus). Ph.D. thesis, Department of Biological Sciences, University of Durham, Durham, UK, 191 pp

  • Gero S (2005) Fundamentals of sperm whale societies: care for calves. M.Sc. thesis, Department of Biology, Dalhousie University, Halifax, Canada, 99 pp

  • Gero S, Gordon J, Carlson C, Evans P, Whitehead H (2007) Population estimate and inter-island movement of sperm whales, Physeter macrocephalus, in the Eastern Caribbean. J Cetacean Res Manage 9:143–150

    Google Scholar 

  • Gordon JCD (1987) Sperm whale groups and social behaviour observed off Sri Lanka. Rep Int Whal Comm 37:205–217

    Google Scholar 

  • Gowans S, Whitehead H, Hooker SK (2001) Social organization in northern bottlenose whales, Hyperoodon ampullatus: not driven by deep-water foraging? Anim Behav 62:369–377

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–52

    Article  PubMed  CAS  Google Scholar 

  • Hauser MD, Tyrell G (1984) Old age and its behavioural manifestations: a study on two species of macaque. Folia Primatol 43:24–35

    Article  PubMed  CAS  Google Scholar 

  • Hawkes K, O’Connell JF, Blurton-Jones NG, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95:1336–1339

    Article  PubMed  CAS  Google Scholar 

  • Hemelrijk CK (1990) Models and tests for reciprocity, unidirectionality and other social interaction patterns at a group level. Anim Behav 39:1013–1029

    Article  Google Scholar 

  • Hinde RA (1976) Interactions, relationships, and social structure. Man 11:1–17

    Article  Google Scholar 

  • Hill K, Hurtado AM (1991) The evolution of reproductive senescence and menopause in human females. Hum Nature 2:313–250

    Article  Google Scholar 

  • Hoelzel AR (1998) Molecular genetic analysis of populations. Oxford University Press, Oxford, UK

    Google Scholar 

  • Hrdy SB (1981) Nepotists and altruists: the behavior of old female among macaques and langur monkeys. In: Amoss PT, Harreli S (eds) Other ways of growing old: anthropological perspectives. Standford University Press, Stanford, CA, pp 59–76

    Google Scholar 

  • Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48:215–267

    Article  Google Scholar 

  • Jefferson TA, Stacey PJ, Baird RW (1991) A review of killer whale interactions with other marine mammals: predation to co-existence. Mamm Rev 4:151–180

    Article  Google Scholar 

  • Karczmarski L, Wursig B, Gailey G, Larson KW, Vanderlip C (2005) Spinner dolphins in a remote Hawaiian atoll: social groupings and population structure. Behav Ecol 16:675–685

    Article  Google Scholar 

  • Lee PC (1987) Allomothering among African elephants. Anim Behav 35:278–291

    Article  Google Scholar 

  • Lettevall E, Richter C, Jaquet N, Slooten E, Dawson S, Whitehead H, Christal J, Howard PM (2002) Social structure and residency in aggregations of male sperm whales. Can J Zool 80:1189–1196

    Article  Google Scholar 

  • Lyrholm T, Gyllensten U (1998) Global matrilineal population structure in sperm whales as indicated by mitochondrial DNA sequences. Proc R Soc Lond B 265:1679–1684

    Article  CAS  Google Scholar 

  • Mann J, Smuts BB (1998) Natal attraction: allomaternal care and mother infant separations in wild bottlenose dolphins. Anim Behav 55:1097–1113

    Article  PubMed  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Maxim PE (1979) Social behavior. In: Bowden DM (ed) Aging in nonhuman primates. Van Nostrand Reinhold, New York, pp 56–70

    Google Scholar 

  • Mesnick SL (2001) Genetic relatedness in sperm whales: evidence and culture implications. Behav Brain Sci 24:346–347

    Article  Google Scholar 

  • Mesnick SL, Evans K, Taylor BL, Hyde J, Escorza-Trevino S, Dizon AE (2003) Sperm whale social structure: why it takes a village to raise a child. In: de Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, pp 170–174

    Google Scholar 

  • Miklós I, Podani J (2004) Randomization of presence–absence matrices: comments and new algorithms. Ecology 85:86–92

    Article  Google Scholar 

  • Nakamichi M (1984) Behavioral characteristics of old female Japanese monkeys in a free-ranging group. Primates 25:192–203

    Article  Google Scholar 

  • Newton-Fisher NE (1999) Associations by male chimpanzees: a social tactic? Behaviour 136:705–730

    Article  Google Scholar 

  • Nicolson NA (1987) Infants, mothers, and other females. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, IL, pp 330–342

    Google Scholar 

  • Owen ECG, Wells RS, Hofmann S (2002) Ranging and association patterns of paired and unpaired adult male Atlantic bottlenose dolphins, Tursiops truncatus, in Sarasota, Florida, provide no evidence for alternative male strategies. Can J Zool 80:2072–2089

    Article  Google Scholar 

  • Palsbøll PJ, Bérubé M, Larsen F, Jorgensen H (1997) Primers for the amplification of tri- and tertamer microsatellite loci in baleen whales. Mol Ecol 6:893–895

    Article  PubMed  Google Scholar 

  • Pavelka MSM (1991) Sociability in old female Japanese monkeys: human versus nonhuman primate aging. Am Anthropol 93:588–598

    Article  Google Scholar 

  • Pitman RL, Ballance LT, Mesnick SL, Chivers SJ (2001) Killer whale predation on sperm whales: observations and implications. Mar Mamm Sci 17:494–507

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Rice D (1989) Sperm whale, Physeter macrocephalus Linnaeus, 1758. In: Ridgeway SH, Harrison R (eds) Handbook of marine mammals: river dolphins and the larger toothed whales. vol. 4. Academic, London

    Google Scholar 

  • Richard KR, Dillon MC, Whitehead H, Wright JM (1996a) Patterns of kinship in groups of free-living sperm whales (Physeter macrocephalus) revealed by multiple molecular genetic analyses. Proc Natl Acad Sci USA 93:8792–8795

    Article  PubMed  CAS  Google Scholar 

  • Richard KR, Whitehead H, Wright JM (1996b) Polymorphic microsatellites from sperm whales and their use in the genetic identification of individuals from naturally sloughed pieces of skin. Mol Ecol 5:313–315

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP, Merrit DB, Derr JN (1999) Microsatellite diversity in captive bottlenose dolphins (Tursiops truncatus). J Hered 90:228–231

    Article  PubMed  CAS  Google Scholar 

  • Schulz T (2007) The production and exchange of sperm whale coda vocalizations. Ph.D. thesis, Department of Biology, Dalhousie University, Halifax, Canada, 249pp

  • Schnell GD, Watt DJ, Douglas ME (1985) Statistical comparison of proximity matricies: applications in animal behaviour. Anim Behav 33:239–253

    Article  Google Scholar 

  • Schusterman RJ, Reichmuth CJ, Kastak D (2000) How animals classify friends and foes. Curr Dir Psychol Sci 9:1–6

    Article  Google Scholar 

  • Sidman M (1994) Equivalence relations and behavior: a research story. Authors Cooperative, Boston, MA

    Google Scholar 

  • Silk JB (2005) Practicing Hamilton’s rule: kin selection in primates groups. In: Kappeler PM, Van Schaik CP (eds) Cooperation in primates and humans: mechanisms and evolution. Springer, New York, pp 25–46

    Google Scholar 

  • Stookey JM, Gonyou HW (1998) Recognition in swine: recognition through familiarity or genetic relatedness? Appl Anim Behav Sci 55:291–305

    Article  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Valsecchi E, Amos W (1996) Microsatellite markers for the study of cetacean populations. Mol Ecol 5:151–156

    Article  PubMed  CAS  Google Scholar 

  • Vonhof MJ, Whitehead H, Fenton MB (2004) Analysis of Spix’s disc-winged bat association patterns and roosting home ranges reveal a novel social structure among bats. Anim Behav 68:507–521

    Article  Google Scholar 

  • Waser PM (1978) Postreproductive survival and behavior in a free-ranging female mangabey. Folia Primatol 29:142–160

    Article  PubMed  CAS  Google Scholar 

  • Weilgart L, Whitehead H, Payne K (1996) A colossal convergence. Am. Scientist 84:278–287

    Google Scholar 

  • Whitehead H (1989) Formations of foraging sperm whales, Physeter macrocephalus, off the Galapagos Islands. Can J Zool 67:2131–2139

    Article  Google Scholar 

  • Whitehead H (1990) Computer assisted individual identification of sperm whale flukes. Rep Int Whal Comm Spec Issue 12:71–77

    Google Scholar 

  • Whitehead H (1993) The behavior of mature male sperm whales on the Galapagos Islands breeding grounds. Can J Zool 71:689–699

    Google Scholar 

  • Whitehead H (1996) Babysitting, dive synchrony, and indications of alloparental care in sperm whales. Behav Ecol Sociobiol 38:237–244

    Article  Google Scholar 

  • Whitehead H (2003) Sperm whales: social evolution in the ocean. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Whitehead H (2008a) Programs for analysing social structure: SOCPROG 2.3 manual. http://myweb.dal.ca/hwhitehe/MANUAL.htm

  • Whitehead H (2008b) Precision and power in the analysis of social structure using associations. Anim Behav 75:1093–1099

    Article  Google Scholar 

  • Whitehead H, Dufault S (1999) Techniques for analysing vertebrate social structure using identified individuals: review and recommendations. Adv Stud Behav 28:33–74

    Article  Google Scholar 

  • Whitehead H, Gordon J, Mathews EA, Richard KR (1990) Obtaining skin samples from living sperm whales. Mar Mamm Sci 6:316–326

    Article  Google Scholar 

  • Whitehead H, Christal J, Dufault S (1997) Past and distant whaling and the rapid decline of sperm whales off the Galapagos Islands. Conserv Biol 11:1387–1396

    Article  Google Scholar 

  • Whitehead H, Bejder L, Ottensmeyer CA (2005) Testing association patterns: issues arising and extensions. Anim Behav 69:e1–e6

    Article  Google Scholar 

  • Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Article  Google Scholar 

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Acknowledgements

Research in Dominica was carried out under a scientific research permit (SCR 013/05-02) provided by the Ministry of Agriculture and Environment of Dominica. We would like to thank all of Balaena’s crew members, Andrew Amour and the staff at the Anchorage Hotel and Dive Center for critical logistical support while in Dominica and Ron Burns at Northwoods DNA for completing much of the genetic lab work. Erica Johnson, Marie Auger-Méthé, Devin Lyons, and two anonymous reviewers each provided helpful comments on this manuscript. We also thank Jens Krause for drawing our attention to the work of Miklós and Podani (2004). This project was supported by operating and equipment grants to H.W. from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Whale and Dolphin Conservation Society, to Luke Rendell from the UK Natural Environment Research Council, and S.G. was supported during the course of this study by an NSERC Postgraduate Scholarship (PGS-M). To the knowledge of the authors, this research complies with the current laws of the Commonwealth of Dominica.

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  1. Dan Engelhaupt

    Present address: , P.O. Box 197, Picton, New Zealand

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  1. Department of Biology, Dalhousie University, Halifax, NS, B3H 4J1, Canada

    Shane Gero & Hal Whitehead

  2. Department of Biological Sciences, University of Durham, South Road, Durham, DH1 3LE, UK

    Dan Engelhaupt

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  1. Shane Gero
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Gero, S., Engelhaupt, D. & Whitehead, H. Heterogeneous social associations within a sperm whale, Physeter macrocephalus, unit reflect pairwise relatedness. Behav Ecol Sociobiol 63, 143–151 (2008). https://doi.org/10.1007/s00265-008-0645-x

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