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Summary In polygynous and polygynandrous species, there is often intense male-male competition over access to females, high male reproductive skew, and more male investment in mating effort than parenting effort [ 1 ]. However, the benefits derived from mating effort and parenting effort may change over the course of males’ lives. In many mammalian species, there is a ∩-shaped relationship between age, condition, and resource holding power as middle-aged males that are in prime physical condition outcompete older males [ 2 , 3 , 4 , 5 , 6 , 7 , 8 ] and sire more infants [ 9 , 10 , 11 , 12 ]. Thus, males might derive more benefits from parenting effort than mating effort as they age and their competitive abilities decline [ 13 ]. Alternatively, older males may invest more effort in making themselves attractive to females as mates [ 14 ]. One way that older males might do so is by developing relationships with females and providing care for their offspring [ 14 , 15 ]. Savannah baboons provide an excellent opportunity to test these hypotheses. They form stable multi-male, multi-female groups, and males compete for high ranking positions. In yellow and chacma baboons (Papio cynocephalus and P. ursinus), there is a ∩-shaped relationship between male age and dominance rank [ 12 ], and high rank enhances paternity success [ 12 , 16 ]. Lactating female baboons form close ties (“primary associations” hereafter) with particular males [ 15 , 16 , 17 , 18 , 19 , 20 ], who support them and their infants in conflicts [ 15 , 19 ] and buffer their infants from rough handling [ 20 ]. Females’ primary associates are often, but not always, the sires of their current infants [ 16 , 20 , 21 , 22 ].

In polygynous species, there is often intense intra-sexual competition over access to females and high reproductive skew, and males invest more in mating effort than parenting effort. However, the benefits of investments in mating effort and parenting effort may change systematically over the course of males’ lives. In many polygynous mammalian species, there is an ∩-shaped relationship between age, condition, and resource holding power as middle-aged males that are in prime physical condition outcompete older and younger males. As males age, and their competitive abilities decline, males might benefit from reallocating investment from mating effort to parenting effort. We examined the effects of male age and paternity on the likelihood that male olive baboons, Papio anubis, would invest in parenting effort. Male baboons compete for high ranking positions in the group, and there is an ∩-shaped relationship between male age and dominance rank. High ranking males sire more infants than lower ranking males. Males and lactating females often form close ties (primary associates), and females’ primary associates are likely to be the sires of their infants. Males are attentive to their primary associates’ distress, support them in conflicts, and buffer their infants from rough handling and harassment. Here, we show that males are more likely to become the primary associates of lactating females as they age and their competitive abilities decline. These results suggest that fitness benefits derived from male parental investment may favor an extended post-reproductive lifespan in species in which males can identify their own offspring and positively affect their welfare.

Long-term male-female bonds and bi-parental investment in offspring are hallmarks of human society. A key question is how these traits evolved from the polygynandrously mating multimale multifemale society that likely characterized the Pan-Homo ancestor. In all three species of savanna baboons, lactating females form strong ties (sometimes called "friendships") with one or more adult males. For yellow baboons (Papio cynocephalus) and chacma baboons (Papio ursinus), several lines of evidence suggest that these relationships are a form of male parenting effort. In olive baboons (Papio anubis), females are thought to preferentially mate with their "friends", and male-female bonds may thus function as a form of mating effort. Here, we draw on behavioral and genetic data to evaluate the factors that shape male-female relationships in a well-studied population of olive baboons. We find support for the parenting effort hypothesis in that sires have stronger bonds with their infants' mothers than do other males. These bonds sometimes persist past weaning age and, in many cases, the sire of the previous infant is still a close partner of the female when she nurses her subsequent offspring. We find that males who have the strongest bonds with females that have resumed cycling, but are not currently sexually receptive, are more likely to sire the female's next offspring but the estimate is associated with large statistical uncertainty. We also find that in over one third of the cases, a female's successive infants were sired by the same male. Thus, in olive baboons, the development of stable breeding bonds and paternal investment seem to be grounded in the formation of close ties between males and anestrous females. However, other factors such as male dominance rank also influence paternity success and may preclude stability of these bonds to the extent found in human societies.

In many social animals, individuals derive fitness benefits from close social bonds, which are often formed among kin of the philopatric sex. Hamadryas baboons, however, exhibit a hierarchical, multilevel social system where both sexes disperse from their natal one-male-unit (OMU). Although this would seem to hinder maintenance of kin ties, both sexes appear largely philopatric at the higher order band and clan levels, possibly allowing for bonds with same sex kin by both males and females. In order to investigate the possibility of kin bonds in hamadryas baboons, we identified kin dyads in a band without known pedigree information using a large panel of genetic markers: 1 Y-linked, 4 X-linked, and 23 autosomal microsatellites and part of the mitochondrial hypervariable region I. With these data, we performed a kinship analysis while accounting for misclassification rates through simulations and determined kinship among two types of dyads: leader and follower males and female dyads within OMUs. Leader and follower males were maternal relatives more often than expected by chance, suggesting that kinship plays a role in the formation of these relationships. Moreover, maternal female relatives were found in the same OMU more often than expected by chance, indicating that females may be motivated to maintain post-dispersal contact with maternal female kin. Our results suggest that hamadryas baboons can recognize maternal kin and that kin selection has contributed to shaping their complex social system. This implies that an ancestral maternal kin bias has been retained in hamadryas society. Am. J. Primatol. 78:731-744, 2016. © 2016 Wiley Periodicals, Inc.