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The Evolution of Behaviors Regulating Density and Age-Specific Sex Ratios in a Primate Population

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Adult females within a macaque troop are related to one another and to all infants and juveniles. Thus, the evolution of social behaviors that impose mortality differentially by age and sex is interpreted in light of classical and kin selection. Parental and kin investment are defined and measured by the degree to which dominant relatives tolerate (closely associate with but do not exploit) subordinate relatives during foraging; and, by the degree to which subordinate relatives are exploited for resources by their dominant relatives. Sex differences in mortality among juveniles and infants are the outcome of differences in parental and kin investments which are geared to maximize fitness according to sex differences in reproductive strategy. Relative to females, males grow faster during youth, and acquire larger adult size and a greater ability to compete for mates. Males also suffer higher mortality as adults and particularly during adolescence when males emigrate from the maternal troop and when the attributes necessary for male reproductive success develop most. Such differences probably evolved through intrasexual selection. Investment involves offsetting mortality occurring in males after they emigrate from the maternal troop by investing in them heavily prior to their emigration so as to maximize their chances of survival and development to reproductive age and state. This is achieved at the expense of investment in their infant and juvenile female peers, which consequently suffer greater mortality than do infant and juvenile males. Males, however, must emigrate at adolescence to prevent additional investment in them at the further expense of related female peers. By emigrating, adolescent males safeguard the kinship component of their inclusive fitness and gain an opportunity to improve their otherwise jeopardized individual fitness in a new social setting. The relatively low investment in females during the infant and juvenile period is balanced or compensated to equal that in males by continued investment in them through adulthood, as females do not emigrate from their maternal troop. Thus, total investment in the sexes is equal and parents and kin gain equal fitness through male and female progeny and kin. The male and female cohorts utilize contested resources equally. Altruistic and exploitative behavioral relations between related or unrelated males and females are explained on the basis of a balance between cost and benefit in fitness (classical and inclusive) that these behavioral relations confer. Relative to equilibrium conditions (Ro = 1), when food supply decreases (Ro<1), mortality increases among the infants and youngest juveniles, and among female relative to male juveniles; whereas under food surplus (Ro>1) survivorship among these animals improves. Thus, when the availability of limiting resources changes, the effects of parental and kin investments on growth and survivorship, and probably their nature, change as well, so as to maximize fitness under the new conditions. I propose that the regulation of population size and age-sex distribution is an outcome of classical and kin selected (aggressive and affiliative) behaviors that (1) influence growth rates and impose mortality by determining access to vital resources and estrous females differentially by age, sex and the degree of relatedness, r; (2) function to maximize the classical fitness of unrelated animals and the inclusive fitness of related troop members in accordance with reproductive strategy and the availability of limiting resources; and (3) results in bringing the troop size and population size into equilibrium with the availability of food resources and non-socially imposed mortality. Though scant, data from other species are in accord with those from M. sinica, thereby suggesting a broader relevance of the hypotheses and conclusions set forth in this paper. For example, as parental and kin investment are geared to maximize fitness according to the degree of sexual dimorphism, it is reasonable to expect parental and kin investment behaviors, and thence the age-specific sex ratios, to vary according to the magnitude of the difference in sexual dimorphism in size and mating strategy. A monomorphic mating system (as in lemurs and gibbons) predictably would require a minimum of difference in parental and kin investment behaviors by sex, and sex ratios should therefore tend forwards equality at all ages. But, in highly dimorphic species (e.g., patas monkeys and baboons) differences in parental and kin investment in male and female offspring and kin would be accentuated, such that the need to develop large adult male size, for example, might be compensated for by decreasing the number of males among adults. Comparative data support these implications. Other selective pressures, concerning for example, trophic adaptations, might limit the effects of intrasexual selection on the degree of sexual dimorphism, and in this indirect way influence investment behaviors and age-specific sex ratios. Similarly, niche adaptations that are specific to one age or sex only may alter the age and sex ratios in favor of the age-sex class exclusively benefiting from the additionally exploitable resource. Thus, reproductive strategies, trophic and similar life-sustaining adaptations and the availability of limiting resources influence social behaviors which determine the age-specific sex ratios of the population.

Affiliations: 1: Office of Zoological Research, National Zoological Park, Smithsonian Institution, Washington, D.C., U.S.A.


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