Paternity alone does not predict long-term investment in juveniles by male baboons

Liza R. Moscovice 0 1 2 Marlies Heesen 0 1 2 Anthony Di Fiore 0 1 2 Robert M. Seyfarth 0 1 2 Dorothy L. Cheney 0 1 2 0 A. Di Fiore Department of Anthropology, New York University , New York, NY 10003, USA 1 M. Heesen Junior Research Group on Primate Socio-ecology, Max Planck Institute for Evolutionary Anthropology , 14103 Leipzig, Germany 2 R. M. Seyfarth Department of Psychology, University of Pennsylvania , Philadelphia, PA 19104-6241, USA Adult male chacma baboons (Papio hamadryas ursinus) form preferential associations, or friendships, with particular lactating females. Males exhibit high levels of affiliative contact with their friends' infants and defend them from potentially infanticidal attacks (Palombit et al. 1997). Little is known about males' associations with juveniles once they have passed the period of infanticidal risk. We conducted an observational, experimental, and genetic study of adult male and juvenile chacma baboons in the Moremi Reserve, Botswana. We identified preferential associations between males and juveniles and used behavioral data and a playback experiment to explore whether those associations have potential fitness benefits for juveniles. We determined whether males preferentially invest in care of their own offspring. We also determined how often males invest in care of their former friends' offspring. The majority of juveniles exhibited preferential associations with one or two males, who had almost always been their mother's friend during infancy. However, in only a subset of these relationships was the male the actual father, in part because many fathers died or disappeared before their offspring were weaned. Male caretakers intervened on behalf of their juvenile associates in social conflicts more often than they intervened on behalf of unconnected juveniles, and they did not appear to differentiate between genetic offspring and unrelated associates. Playbacks of juveniles' distress calls elicited a stronger response from their caretakers than from control males. Chacma males may provide care to unrelated offspring of former friends because the costs associated with such care are low compared with the potentially high fitness costs of refusing aid to a juvenile who is a possible offspring. - Male chacma baboons (Papio hamadryas ursinus), like males in other baboon subspecies, form close preferential associations, or friendships, with lactating females that coincide with infant birth and terminate abruptly if the infant dies (Palombit et al. 1997, 2000). Chacma infants face higher rates of infanticide than East African conspecifics, and male friends can have a significant impact on infant survival (Palombit et al. 2000; Weingrill 2000). Behavioral and experimental studies indicate that chacma males are more willing to protect female friends than nonfriends when threatened by potentially infanticidal males (Palombit et al. 1997). During periods of high infanticidal risk, lactating females with a male friend exhibit a reduced stress response compared with lactating females without a male friend (Beehner et al. 2005; Engh et al. 2006), underscoring the importance of friendships as infanticide deterrents from the females perspective. There has been little research on chacma males relationships with immature baboons after their female friends resume cycling, when offspring are no longer at high risk of infanticide. In yellow baboons (Papio hamadryas cynocephalus) co-residency with male caretakers has important short- and long-term fitness implications for juveniles. Males aid their offspring in aggressive disputes significantly more often than they aid unrelated juveniles (Buchan et al. 2003). Furthermore, the presence of a father during the juvenile period significantly accelerates the age of maturation for both males and females (Charpentier et al. 2008). These studies suggest more extensive and long-term paternal care than has previously been reported in Old World monkeys (e.g., Stein 1984, Taub and Redican 1984). It remains unclear how males determine the recipients of their caretaking behavior. Yellow baboon males appear to distinguish genetic offspring from unrelated juveniles, even when they mated with the mothers of unrelated juveniles during their conceptive cycles (Buchan et al. 2003). Such discrimination is consistent with phenotypic matching, but it could also result from behavioral cuesfor example, memory of the proportion of a females consort days that the male monopolized, or a previous friendship with the juveniles mother. We designed a study to examine male chacma baboons relationships with juveniles once they have passed the period of high infanticidal risk. Chacma baboon friendships are characterized by high levels of affiliative contact between males and their friends infants, including frequent infant carrying (Busse and Hamilton 1981; Palombit et al. 1997). These close associations may promote a long-term bond between a male and the offspring of his female friend that continues after the female resumes cycling and no longer associates closely with her former friend (Palombit et al. 1997). If malefemale friendships facilitate long-term bonds between males and particular juveniles, males should invest in their former friends offspring regardless of their genetic relatedness to them. Because male chacma baboons typically form friendships with previous consort partners (Palombit et al. 2000; Weingrill 2000; Moscovice et al., manuscript in preparation), investment in the juvenile offspring of former friends should then also frequently result in paternal care. Alternatively, males might provide preferential care only to their genetic offspring, irrespective of their previous friendships with particular females. This outcome would be consistent with patterns of male care of juveniles in yellow baboons and would offer further support for phenotypic matching. In this paper, we identify preferential associations between males and juveniles and examine whether male caretaking behavior is directed preferentially toward genetic offspring. We also compare malejuvenile associations with males previous associations with the juveniles mothers during lactation to test the hypothesis that males may use behavioral cues from previous friendships to determine patterns of investment in juveniles. Finally, we use behavioral data and a playback experiment to explore whether associations with male caretakers have potential fitness benefits for juveniles. Materials and methods Study site and population Subjects were members of a group of wild chacma baboons living in the Moremi Game Reserve in the Okavango Delta of Botswana. The group has been observed since 1978 and has been the subject of intensive behavioral observation since mid-1992. All births and deaths, as well as immigration and emigration, are noted daily and matrilineal relatedness of all individuals is known (Cheney et al. 2004). Female baboons usually attain a rank sim (...truncated)