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Parent–Offspring Conflict in Primates

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Parent–Offspring Conflict in Primates P1: Vendor/GCQ/GIR P2: GDX International Journal of Primatology [ijop] pp425-ijop-369512 May 11, 2002 15:56 Style file version Nov. 19th, 1999 International Journal of Primatology, Vol. 23, No. 4, August 2002 (C 2002) Parent–Offspring Conflict in Primates Dario Maestripieri1 Received February 19, 2001; accepted September 12, 2001 Parent–offspring conflict (POC) theory (Trivers, 1974) has stimulated con- troversy in evolutionary biology and behavioral ecology. The theory has been criticized by some primate behavioral researchers on both conceptual and em- pirical grounds. First, it has been argued that it would be more advantageous to mothers and offspring to agree over the allocation of parental investment and to cooperate rather than to disagree and engage in conflict. Second, some stud- ies have provided data suggesting that primate mothers and offspring engage in behavioral conflict over the scheduling of their activities rather than parental investment. In reality, parent–offspring interactions are likely to involve both cooperation and conflict, and the hypothesis that mothers and infants squab- ble over the scheduling of their activities is not incompatible with POC theory. Furthermore, the predictions of POC theory are supported by a number of empirical studies of primates. POC theory has enhanced our understanding of the dynamics of parent–offspring relationships in many animal species, and it is very likely that future studies of primates will continue to benefit from using POC theory as an explanatory framework. KEY WORDS: parent–offspring conflict; parental investment; timing hypothesis; primates. PARENT–OFFSPRING CONFLICT THEORY Trivers (1972) defined parental investment (PI) as any investment by the parent in an individual offspring that increases its chance of surviving and hence reproductive success at the cost of the parent’s ability to invest in other offspring. In a seminal paper on the evolution of parent–offspring 1Committee on Evolutionary Biology, The University of Chicago, 5730 S. Woodlawn Avenue, Chicago, Illinois 60637; e-mail: [email protected]. 923 0164-0291/02/0800-0923/0 C 2002 Plenum Publishing Corporation P1: Vendor/GCQ/GIR P2: GDX International Journal of Primatology [ijop] pp425-ijop-369512 May 11, 2002 15:56 Style file version Nov. 19th, 1999 924 Maestripieri conflict (POC), Trivers (1974) argued that offspring are selected to demand more investment than parents are selected to give. In his view, the ensuing behavioral conflict over PI is caused by a genetic conflict of interests because whereas parents are equally related to all of their offspring and selected to balance investment among their current and future offspring, the offspring are only half related to their siblings and therefore are selected to demand investment from their parents even at their siblings’ expense. Trivers (1974) argued that behavioral conflict between parents and offspring should occur over the termination of PI, with offspring demanding a longer investment period, as well as over the amount of investment to be provided at any time during the period of offspring dependence. Trivers’ POC theory has stimulated substantive controversy in behav- ioral and evolutionary biology (Mock and Forbes, 1992; Godfray, 1995; Stamps, 1980). After some initial skepticism about the theory’s scientific va- lidity (Alexander, 1974), subsequent theoretical models showed that POC can indeed evolve and be maintained in a population by natural selection (Parker and MacNair, 1978). Unfortunately, many of the models did not make specific predictions about the behavior of parents and offspring and therefore have been difficult to test (Godfray,1995). Mock and Forbes (1992) pointed out that attempts to test POC theory empirically have also been hin- dered by the inherent difficulty of measuring PI, the flawed assumption that PI optima of parents and offspring are only determined by asymmetries in genetic relatedness, and the fact that only results showing that offspring win the conflict can constitute unambiguous demonstration of phenotypic POC because a parental win is the default result by virtue of the power asymmetry between parents and offspring. Although mother–offspring behavioral conflict has been documented in a wide range of mammals and birds, some authors have warned against the risk of overinterpreting the behaviors (Godfray, 1995) or have explicitly questioned the notion that behavioral conflict reflects evolutionary conflict of interest (Altmann, 1980; Bateson, 1994). For example, Bateson (1994) argued that conflict between mother and offspring in many species of ani- mals occurs at stages other than weaning, that offspring often appear to wean themselves, and that mothers and offspring monitor each other and act in the common interest rather than engaging in competition or conflict. In a reply to Bateson (1994), Svensson (1995) pointed out that even though mother and offspring monitor each other and often exchange mutually advantageous in- formation, their optimal amount of PI may still differ. Therefore, neither the notion of mother-infant monitoring and cooperation nor the empirical find- ings cited by Bateson (1994) are necessarily incompatible with POC theory. POC theory was stimulated by observations of intense behavioral con- flict between parents and offspring in birds and primates (Trivers, 1985). The P1: Vendor/GCQ/GIR P2: GDX International Journal of Primatology [ijop] pp425-ijop-369512 May 11, 2002 15:56 Style file version Nov. 19th, 1999 Parent–Offspring Conflict in Primates 925 offspring solicit resources from their parents in ways that appear energet- ically costly or that risk attracting predators. Furthermore, primate infants often engage in squabbles with their parents that may continue for a number of years. Although primates would appear to be ideal subjects to investigate POC theory empirically, most primate studies have actually challenged POC theory rather than supported it. In this article, I re-evaluate the testing of POC theory with primate data by describing mother-infant behavioral conflict in different species and then reviewing studies of POC in relation to whether the researchers interpreted their findings as inconsistent or consistent with Trivers’ theory. MOTHER–OFFSPRING BEHAVIORAL CONFLICT IN PRIMATES Behavioral conflict occurs in most species of primates in which parent– offspring interactions have been carefully studied. Quantitative information about the phenomenon is limited for prosimians and New World monkeys (Ehrlich and MacBride, 1989; Gould, 1990; Ingram, 1977; Locke-Haydon and Chalmers, 1983). Behavioral conflict has been well documented in some species of Old World monkeys and apes. Observations of maternal rejections and infant distress responses in lan- gurs and baboons were reported by Jay (1963), DeVore (1963), and other field workers. In Jay’s (1965) study, langur mothers alternated for weeks between rejecting their infants and allowing them to cling. A few mothers began to reject their infants after only 1 mo, whereas others females did not reject their infants until they resumed estrus. All females intensified their rejections when they returned to estrus. Like langurs, baboon mothers ob- served by DeVore (1963) increasingly rejected their infants upon resumption of estrus. Rejected infants gave loud cries and intensified their attempts to cling to their mothers and to nurse. Ransom and Rowell (1972) reported that some baboon mothers began rejections at postpartum week 10 whereas oth- ers did so at 35 weeks, when they resumed estrus. Rejection was occasionally accompanied by aggression. According to Nash (1978), maternal aggression in baboons occurred in 3 main contexts: weaning of suckling, resistance to the infant’s riding, and mating activity. In her study, maternal aggres- sion, rejection, and tantrums peaked at the same time and conflict was most intense in conjunction with the mother’s mating activity. Unlike previous baboon researchers, Altmann (1980) mentioned no behavioral conflict oc- curring after the mother’s resumption of estrus. Instead, she emphasized that mothers often rejected contact attempts made by the infants during foraging and, to a lesser extent, during travelling and resting. In macaques, maternal P1: Vendor/GCQ/GIR P2: GDX International Journal of Primatology [ijop] pp425-ijop-369512 May 11, 2002 15:56 Style file version Nov. 19th, 1999 926 Maestripieri rejections can begin as early as the first month of infant life and peak between 10 and 12 mo of age (Hinde and Spencer-Booth, 1967; Maestripieri, 1994a). The most common contexts for mother-infant behavioral conflict include travel (Johnson, 1986), feeding (Rosenblum and Sunderland, 1982), the for- mation of sleeping clusters (Hammerschmidt et al., 1994) and the mother’s resumption of mating (Berman et al., 1993; Collinge, 1987; Gomendio, 1991; Worlein et al., 1988). Mother-infant behavioral conflicts in the great apes have been described as intense and prolonged. In orangutans, the first signs of conflict occurred at 5 mo of age and continued for several years; conflicts with older offspring often included violent screaming and aggression (Horr, 1977). Behavioral conflicts were most common during daytime feeding and at the time of nest building, particularly when mothers had newborn and ejected previ- ous offspring from the nest. In chimpanzees, mother-infant conflicts occur during feeding, grooming, travelling, evening nesting, suckling, and mating (Clark, 1977; Goodall, 1968; Horvat and Kraemer, 1982; Pusey, 1983; van de Rijt-Plooij and
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