Trade-offs in primate grooming reciprocation: testing behavioural flexibility and correlated evolution

Primates may trade altruistic behaviours, such as grooming, either for itself or for different rank-related benefits, such as tolerance or agonistic support. Ecological conditions are expected to affect competition and thus the steepness of dominance hierarchies. This, in turn, may influence the value of the different currencies that primates exchange. Thus, it can be hypothesized that, as the dominance hierarchy becomes steeper, more grooming is directed up the hierarchy (in exchange for tolerance or agonistic support) and less grooming is exchanged for other grooming. We assembled a large database of within-group grooming distribution in primates (38 social groups belonging to 16 species and eight genera) and tested these hypotheses both within species (i.e. comparing different groups of the same species) and between species (using comparative methods that control for phylogenetic relatedness). We found within-species evidence that steeper dominance hierarchies were associated with more grooming being directed up the hierarchy, and that a trade-off occurred between the tendency to groom up the hierarchy and the degree of grooming reciprocation (although, in some analyses, only a nonsignificant trend was observed). By contrast, phylogenetically controlled comparisons between species did not reveal evidence of correlated evolution between the steepness of the dominance hierarchy, the tendency to direct grooming up the hierarchy, and the degree of grooming reciprocation.

[1]  S. Peter Henzi,et al.  A dynamic interaction between aggression and grooming reciprocity among female chacma baboons , 2002, Animal Behaviour.

[2]  A. Purvis A composite estimate of primate phylogeny. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  B. Majolo,et al.  Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support , 2006, American journal of primatology.

[4]  B. Chapais,et al.  Differential effects of kinship, dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata , 1988, Primates.

[5]  Eric B. Keverne,et al.  Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships , 1989, Psychoneuroendocrinology.

[6]  Gabriele Schino,et al.  Grooming, competition and social rank among female primates: a meta-analysis , 2001, Animal Behaviour.

[7]  Filippo Aureli,et al.  Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. , 1999, Journal of comparative psychology.

[8]  H. Vries The rowwise correlation between two proximity matrices and the partial rowwise correlation , 1993 .

[9]  Ramón Díaz-Uriarte,et al.  TESTING HYPOTHESES OF CORRELATED EVOLUTION USING PHYLOGENETICALLY INDEPENDENT CONTRASTS: SENSITIVITY TO DEVIATIONS FROM BROWNIAN MOTION , 1996 .

[10]  Gabriele Schino,et al.  Grooming and agonistic support: a meta-analysis of primate reciprocal altruism , 2007 .

[11]  Susan Perry,et al.  Female‐female social relationships in wild white‐faced capuchin monkeys, Cebus capucinus , 1995 .

[12]  P. Whitten,et al.  Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus) , 2006, Proceedings of the Royal Society B: Biological Sciences.

[13]  Yukimaru Sugiyama,et al.  Characteristics of the social life of bonnet macaques (Macaca radiata) , 1971, Primates.

[14]  K. Izawa,et al.  Social behavior of the wild black-capped Capuchin (Cebus apella) , 1980, Primates.

[15]  Charlotte K. Hemelrijk,et al.  Philopatry, male presence and grooming reciprocation among female primates: a comparative perspective , 1998, Behavioral Ecology and Sociobiology.

[16]  D. Sade,et al.  Sociometrics of Macaca mulatta. I. Linkages and cliques in grooming matrices. , 1972, Folia primatologica; international journal of primatology.

[17]  B. Kozintsev,et al.  The structure of affiliative relations in a primate community: Allogrooming in stumptailed macaques (Macaca arctoides) , 1994 .

[18]  Marina Cords,et al.  Old World Monkeys: Agonistic and affiliative relationships in a blue monkey group , 2000 .

[19]  Robin I. M. Dunbar,et al.  Is Social Grooming Altruistic , 2010 .

[20]  Gerald S. Wilkinson,et al.  Social grooming in the common vampire bat, Desmodus rotundus , 1986, Animal Behaviour.

[21]  Odile Petit,et al.  A comparative study of conflict resolution in macaques: insights into the nature of trait covariation , 2008, Animal Behaviour.

[22]  D. Maestripieri Vigilance Costs of Allogrooming in Macaque Mothers , 1993, The American Naturalist.

[23]  Robert M. Seyfarth,et al.  The distribution of grooming and related behaviours among adult female vervet monkeys , 1980, Animal Behaviour.

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

[25]  Naofumi Nakagawa Distribution of affiliative behaviors among adult females within a group of wild patas monkeys in a nonmating, nonbirth season , 1992, International Journal of Primatology.

[26]  B. Gardiner,et al.  Linnean Society of London , 1956, Nature.

[27]  Charlotte K. Hemelrijk,et al.  A matrix partial correlation test used in investigations of reciprocity and other social interaction patterns at group level , 1990 .

[28]  D. Lott,et al.  Intraspecific Variation in the Social Systems of Wild Vertebrates , 1991 .

[29]  K. Zamma Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama , 2007, Primates.

[30]  A. Estrada,et al.  Establishment of a free-ranging colony of stumptail macaques (Macaca arctoides): Social relations I , 1977, Primates.

[31]  C. Nunn,et al.  Comparative methods for studying primate adaptation and allometry , 2001 .

[32]  Lynette A. Hart,et al.  Reciprocal allogrooming in impala, Aepyceros melampus , 1992, Animal Behaviour.

[33]  Clara B. Jones Grooming in the mantled howler monkey,Alouatta palliataGray , 1979, Primates.

[34]  R. Wittig,et al.  Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus) , 2008, Hormones and Behavior.

[35]  D. Maestripieri,et al.  Allogrooming as a tension‐reduction mechanism: A behavioral approach , 1988, American journal of primatology.

[36]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[37]  A. Purvis,et al.  Comparative Primate Socioecology: Phylogenetically independent comparisons and primate phylogeny , 1999 .

[38]  J H Wolfheim,et al.  A quantitative analysis of the organization of a group of captive talapoin monkeys (Miopithecus talapoin). , 1977, Folia primatologica; international journal of primatology.

[39]  R. Seyfarth,et al.  Empirical tests of reciprocity theory: Problems in assessment , 1988 .

[40]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[41]  L. Hedges,et al.  Statistical Methods for Meta-Analysis , 1987 .

[42]  John E. Fa Use of time and resources by provisioned troops of monkeys : social behaviour, time and energy in the barbary macaque (Macaca sylvanus L.) at Gibraltar , 1986 .

[43]  S. Venkatachalam,et al.  Changing social strategies of wild female bonnet macaques during natural foraging and on provisioning , 2003 .

[44]  D. Waal Dominance 'style' and primate social organization , 1989 .

[45]  J. Kaplan,et al.  Social organization in a group of free-ranging patas monkeys. , 1980, Folia primatologica; international journal of primatology.

[46]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[47]  R. A. Hill,et al.  Market forces predict grooming reciprocity in female baboons , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  T. Furuichi,et al.  Comparative study of grooming relationships among wild Japanese macaques in Kinkazan A troop and Yakushima M troop , 1998, Primates.

[49]  N. Koyama Dominance, grooming, and clasped-sleeping relationships among bonnet monkeys in India , 1973, Primates.

[50]  Carel P. van Schaik,et al.  The evolution of female social relationships in nonhuman primates , 1997, Behavioral Ecology and Sociobiology.

[51]  H. Vries,et al.  The influence of the steepness of dominance hierarchies on reciprocity and interchange in captive groups of bonobos (Pan paniscus) , 2005 .

[52]  T. Oi Sociological study on the troop fission of wild , 2006, Primates.

[53]  Andrew Rambaut,et al.  Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data , 1995, Comput. Appl. Biosci..

[54]  V. Sommer,et al.  Weaving a tight social net: Allogrooming in free-ranging female langurs (Presbytis entellus) , 1994, International Journal of Primatology.

[55]  R. Rhine Changes in the social structure of two groups of stumptail macaques (Macaca arctoides) , 1972, Primates.

[56]  D. Blumstein,et al.  The evolution of parasite-defence grooming in ungulates , 2004 .