Social bonds in the dispersing sex: partner preferences among adult female chimpanzees

In most primate societies, strong and enduring social bonds form preferentially among kin, who benefit from cooperation through direct and indirect fitness gains. Chimpanzees, Pan troglodytes, differ from most species by showing consistent female-biased dispersal and strict male philopatry. In most East African populations, females tend to forage alone in small core areas and were long thought to have weak social bonds of little biological significance. Recent work in some populations is challenging this view. However, challenges remain in quantifying the influence of shared space use on association patterns, and in identifying the drivers of partner preferences and social bonds. Here, we use the largest data set on wild chimpanzee behaviour currently available to assess potential determinants of female association patterns. We quantify pairwise similarities in ranging, dyadic association and grooming for 624 unique dyads over 38 years, including 17 adult female kin dyads. To search for social preferences that could not be explained by spatial overlap alone, we controlled for expected association based on pairwise kernel volume intersections of core areas. We found that association frequencies among females with above-average overlap correlated positively with grooming rates, suggesting that associations reflected social preferences in these dyads. Furthermore, when available, females preferred kin over nonkin partners for association and grooming, and variability was high among nonkin dyads. While variability in association above and below expected values was high, on average, nonkin associated more frequently if they had immature male offspring, while having female offspring had the opposite effect. Dominance rank, an important determinant of reproductive success at Gombe, influenced associations primarily for low-ranking females, who associated preferentially with each other. Our findings support the hypothesis that female chimpanzees form well-differentiated social relationships that are of potential adaptive value to females and their offspring.

[1]  John A Updegraff,et al.  Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. , 2000, Psychological review.

[2]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[3]  Jane Goodall,et al.  Noninvasive paternity assignment in Gombe chimpanzees , 2001, Molecular ecology.

[4]  P. Villiers,et al.  Home range, association and related aspects of elephants in the eastern Transvaal Lowveld , 1997 .

[5]  Richard W. Wrangham,et al.  Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation , 2008, Behavioral Ecology and Sociobiology.

[6]  K. Holekamp,et al.  Patterns of Association among Female Spotted Hyenas (Crocuta crocuta) , 1997 .

[7]  B. Hirsch,et al.  Kinship Shapes Affiliative Social Networks but Not Aggression in Ring-Tailed Coatis , 2012, PloS one.

[8]  A. Pusey Sex-biased dispersal and inbreeding avoidance in birds and mammals. , 1987, Trends in ecology & evolution.

[9]  D. Tautz,et al.  Intracommunity relationships, dispersal pattern and paternity success in a wild living community of Bonobos (Pan paniscus) determined from DNA analysis of faecal samples , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  Daniel T. Blumstein,et al.  Social cohesion in yellow-bellied marmots is established through age and kin structuring , 2010, Animal Behaviour.

[11]  J. Bygott Agonistic behaviour and dominance in wild chimpanzees , 1974 .

[12]  C. Boesch,et al.  Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes , 2009, Animal Behaviour.

[13]  D. Watts RECIPROCITY AND INTERCHANGE IN THE SOCIAL RELATIONSHIPS OF WILD MALE CHIMPANZEES , 2002 .

[14]  M. Cords FRIENDSHIP AMONG ADULT FEMALE BLUE MONKEYS (CERCOPITHECUS MITIS) , 2002 .

[15]  C. Boesch,et al.  Y‐chromosome analysis confirms highly sex‐biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus) , 2006, Molecular ecology.

[16]  G. Quinn,et al.  Experimental Design and Data Analysis for Biologists , 2002 .

[17]  J. Goodall,et al.  Boys will be boys: sex differences in wild infant chimpanzee social interactions , 2014, Animal Behaviour.

[18]  S. Lange,et al.  Adjusting for multiple testing--when and how? , 2001, Journal of clinical epidemiology.

[19]  Vincent M. Janik,et al.  Cetacean Societies: Field Studies of Dolphins and Whales , 2001 .

[20]  M. Grove Hunter-gatherer movement patterns: causes and constraints , 2009 .

[21]  Brian P. Farm,et al.  Female competition and male territorial behaviour influence female chimpanzees' ranging patterns , 2002, Animal Behaviour.

[22]  R. Wrangham,et al.  Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression , 2008, Animal Behaviour.

[23]  M. Dahlheim,et al.  Social cohesion among kin, gene flow without dispersal and the evolution of population genetic structure in the killer whale (Orcinus orca) , 2010, Journal of evolutionary biology.

[24]  A. Pusey,et al.  The influence of dominance rank on the reproductive success of female chimpanzees. , 1997, Science.

[25]  A. Pusey,et al.  Early social exposure in wild chimpanzees: Mothers with sons are more gregarious than mothers with daughters , 2014, Proceedings of the National Academy of Sciences.

[26]  Kevin E. Langergraber,et al.  Kinship and social bonds in female chimpanzees (Pan troglodytes) , 2009, American journal of primatology.

[27]  A. Matsumoto-Oda Mahale chimpanzees: Grouping patterns and cycling females , 1999, American journal of primatology.

[28]  A. Pusey,et al.  Female competition in chimpanzees , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[29]  Hilde Vervaecke,et al.  Measuring and testing the steepness of dominance hierarchies , 2006, Animal Behaviour.

[30]  Robin I. M. Dunbar,et al.  Kinship and altruism: a cross-cultural experimental study. , 2007, British journal of psychology.

[31]  F. Campos,et al.  Between-Group Variation in Female Dispersal, Kin Composition of Groups, and Proximity Patterns in a Black-and-White Colobus Monkey (Colobus vellerosus) , 2012, PloS one.

[32]  C. Boesch,et al.  Female gregariousness in Western Chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus , 2013, Behavioral Ecology and Sociobiology.

[33]  Hal Whitehead,et al.  Precision and power in the analysis of social structure using associations , 2008, Animal Behaviour.

[34]  A. Pusey,et al.  Ecology rather than psychology explains co-occurrence of predation and border patrols in male chimpanzees , 2013, Animal Behaviour.

[35]  L. Eberly,et al.  Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes) , 2006 .

[36]  Fitness benefits of coalitionary aggression in male chimpanzees , 2013, Behavioral Ecology and Sociobiology.

[37]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[38]  C. Boesch,et al.  Social influences on ranging patterns among chimpanzees (Pan troglodytes verus) in the Taï National Park, Côte d'Ivoire , 2003 .

[39]  Clément Calenge,et al.  The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals , 2006 .

[40]  J. Mitani,et al.  Male chimpanzees form enduring and equitable social bonds , 2009, Animal Behaviour.

[41]  F. Dobson,et al.  Competition for mates and predominant juvenile male dispersal in mammals , 1982, Animal Behaviour.

[42]  Monica L. Wakefield Social dynamics among females and their influence on social structure in an East African chimpanzee community , 2013, Animal Behaviour.

[43]  Robert A. Gitzen,et al.  Analysis of Animal Space Use and Movements , 2001 .

[44]  Susan C. Alberts,et al.  Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds , 2006, Behavioral Ecology and Sociobiology.

[45]  C. Boesch,et al.  Sexual Differences in Chimpanzee Sociality , 2008, International Journal of Primatology.

[46]  R. Wrangham,et al.  Male–Female Association Patterns Among Free-ranging Chimpanzees (Pan troglodytes schweinfurthii) , 2013, International Journal of Primatology.

[47]  Jean-Michel Gaillard,et al.  Ecological correlates of home‐range size in spring–summer for female roe deer (Capreolus capreolus) in a deciduous woodland , 2005 .

[48]  A. V. Jaarsveld,et al.  Patterns of coalition formation and spatial association in a social carnivore, the African wild dog (Lycaon pictus) , 2003 .

[49]  Elissa Z Cameron,et al.  Social bonds between unrelated females increase reproductive success in feral horses , 2009, Proceedings of the National Academy of Sciences.

[50]  C. D. Kemp,et al.  Density Estimation for Statistics and Data Analysis , 1987 .

[51]  R. Connor,et al.  Complex social structure, alliance stability and mating access in a bottlenose dolphin ‘super-alliance’ , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[52]  Robin I. M. Dunbar,et al.  Cooperation among kin , 2002 .

[53]  R. Wrangham,et al.  Female Competition over Core Areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda , 2008, International Journal of Primatology.

[54]  Ilya R. Fischhoff,et al.  Network metrics reveal differences in social organization between two fission–fusion species, Grevy’s zebra and onager , 2007, Oecologia.

[55]  JOHN FIEBERG,et al.  QUANTIFYING HOME-RANGE OVERLAP: THE IMPORTANCE OF THE UTILIZATION DISTRIBUTION , 2005 .

[56]  A. Pusey,et al.  Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii , 2009, Animal Behaviour.

[57]  Sylvia J. Amsler Energetic costs of territorial boundary patrols by wild chimpanzees , 2009, American journal of primatology.

[58]  Kym P. Patison,et al.  Changes in the group associations of free-ranging beef cows at calving , 2014 .

[59]  N. Kutsukake The Context and Quality of Social Relationships Affect Vigilance Behaviour in Wild Chimpanzees , 2006 .

[60]  Robert M. Seyfarth,et al.  Strong and Consistent Social Bonds Enhance the Longevity of Female Baboons , 2010, Current Biology.

[61]  R. Harcourt,et al.  Shared Reproductive State Enhances Female Associations in Dolphins , 2008 .

[62]  J. Altmann,et al.  Growth rates in a wild primate population: ecological influences and maternal effects , 2005, Behavioral Ecology and Sociobiology.

[63]  Susan C Alberts,et al.  The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants , 2006, Proceedings of the Royal Society B: Biological Sciences.

[64]  R. Wrangham,et al.  Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. , 1980, Journal of reproduction and fertility. Supplement.

[65]  Monica L. Wakefield Grouping Patterns and Competition Among Female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda , 2008, International Journal of Primatology.

[66]  A. Harcourt The Chimpanzees of Gombe. Patterns of Behavior, Jane Goodall. Belknap Press of Harvard University Press, Cambridge, Massachussets (1986), xii, +671. Price $30 , 1988 .

[67]  John W. Pepper,et al.  General Gregariousness and Specific Social Preferences among Wild Chimpanzees , 1999, International Journal of Primatology.

[68]  Anne E. Pusey,et al.  Dominance rank influences female space use in wild chimpanzees, Pan troglodytes: towards an ideal despotic distribution , 2007, Animal Behaviour.

[69]  G. Oehlert,et al.  Influence of Ecological and Social Factors on Body Mass of Wild Chimpanzees , 2005, International Journal of Primatology.

[70]  K. Slocombe,et al.  Female-led infanticide in wild chimpanzees , 2007, Current Biology.

[71]  R. Powell,et al.  An Evaluation of the Accuracy of Kernel Density Estimators for Home Range Analysis , 1996 .

[72]  Sandro Lovari,et al.  Effects of sampling regime on the mean and variance of home range size estimates. , 2006, The Journal of animal ecology.

[73]  R. Wrangham On the evolution of Ape Social Systems , 1979 .

[74]  J. Massen,et al.  Close social associations in animals and humans : functions and mechanisms of friendship , 2010 .

[75]  J. Jones,et al.  Phenotypic quality influences fertility in Gombe chimpanzees. , 2010, The Journal of animal ecology.

[76]  J. Mann,et al.  Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins , 2010, Animal Behaviour.

[77]  Robin I. M. Dunbar The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms , 2010, Neuroscience & Biobehavioral Reviews.

[78]  A. Pusey,et al.  Competing for space: female chimpanzees are more aggressive inside than outside their core areas , 2014, Animal Behaviour.

[79]  A. Pusey Inbreeding avoidance in chimpanzees , 1980, Animal Behaviour.

[80]  R. Wrangham,et al.  Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park , 2007, Animal Behaviour.

[81]  P. Ellison Energetics and reproductive effort , 2003, American journal of human biology : the official journal of the Human Biology Council.

[82]  Francesca Cagnacci,et al.  The home-range concept: are traditional estimators still relevant with modern telemetry technology? , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[83]  Roger Mundry,et al.  Experimental Designs and Data Analysis for Biologists , 2003 .

[84]  Steven J. Schwager,et al.  A comparison of association indices , 1987, Animal Behaviour.

[85]  R. G. Dwyer,et al.  Associations are more strongly correlated with space use than kinship in female eastern grey kangaroos , 2014, Animal Behaviour.

[86]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[87]  A. Pusey,et al.  Severe Aggression Among Female Pan troglodytes schweinfurthii at Gombe National Park, Tanzania , 2008, International Journal of Primatology.

[88]  H. Whitehead,et al.  Heterogeneous social associations within a sperm whale, Physeter macrocephalus, unit reflect pairwise relatedness , 2008, Behavioral Ecology and Sociobiology.

[89]  F. Bercovitch,et al.  Herd composition, kinship and fission–fusion social dynamics among wild giraffe , 2013 .

[90]  C. Packer,et al.  Cooperation and competition within coalitions of male lions: kin selection or game theory? , 1982, Nature.

[91]  Wrangham Rw,et al.  Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. , 1980 .

[92]  A. Pusey,et al.  Behavioural Diversity in Chimpanzees and Bonobos: Costs and benefits of grouping for female chimpanzees at Gombe , 2002 .

[93]  T. Kunz,et al.  Range overlap and association patterns in the tent-making bat Artibeus watsoni , 2007, Animal Behaviour.

[94]  Stewart L. Macdonald,et al.  Structured association patterns and their energetic benefits in female eastern grey kangaroos, Macropus giganteus , 2009, Animal Behaviour.

[95]  M. Cords FRIENDSHIP AMONG ADULT FEMALE BLUE MONKEYS , 2016 .

[96]  E. Otali,et al.  Why chimpanzee (Pan troglodytes schweinfurthii) mothers are less gregarious than nonmothers and males: the infant safety hypothesis , 2006, Behavioral Ecology and Sociobiology.

[97]  L. Vigilant,et al.  Social Bonds Enhance Reproductive Success in Male Macaques , 2010, Current Biology.

[98]  M. Cords,et al.  Socialization of infant blue monkeys (Cercopithecus mitis stuhlmanni): Allomaternal interactions and sex differences , 2005 .

[99]  David Berrigan,et al.  Why do female primates have such long lifespans and so few babies? or Life in the slow lane , 2005 .

[100]  M. E. Thompson Reproductive Ecology of Female Chimpanzees , 2013, American journal of primatology.

[101]  T. Furuichi Social interactions and the life history of femalePan paniscus in Wamba, Zaire , 1989, International Journal of Primatology.

[102]  C. Boesch,et al.  Bisexually bonded ranging in chimpanzees (Pan troglodytes verus) , 2005, Behavioral Ecology and Sociobiology.

[103]  J. Mitani,et al.  Behavioural Diversity in Chimpanzees and Bonobos: Ecological and social correlates of chimpanzee party size and composition , 2002 .

[104]  D. Blumstein,et al.  Social Mating System and Sex-Biased Dispersal in Mammals and Birds: A Phylogenetic Analysis , 2013, PLoS ONE.