The socio-endocrinology of female reproductive strategies in wild Assamese macaques (Macaca assamensis)

Abstract

Sexual conflict is a prominent feature of animals living in multimale-multifemale groups, and drives the evolution of sex-specific reproductive strategies. Owing to divergent reproductive optima, males should compete to monopolize and mate with as many females as possible, whereas females should be more selective of their mates, leading to a coevolutionary arms race between the sexes. Facing the risk of infanticide by males, a source of intense sexual conflict, female primates have evolved counterstrategies and mechanisms to decrease male monopolization potential (i.e. male mating skew) and to manipulate male paternity estimates to overcome the female dilemma , i.e. to balance paternity concentration and dilution. The aim of this thesis was to investigate female reproductive strategies and underlying proximate mechanisms and constraints in a primate with low male contest competition, the Assamese macaque (Macaca assamensis). By combining demographic, behavioral and hormone data, I investigated general female reproductive parameters and life-history traits, and in addition, I visually monitored anogenital sexual swellings in order to investigate their functional significance. I examined female sexual activity and male consortships in relation to fertility, and investigated patterns of reproductive synchrony. I proposed and tested the hypothesis that females behaviorally coordinate their mating activity, and investigated also ovarian cycle synchrony. The study was conducted at Phu Khieo Wildlife Sanctuary in northeastern Thailand during two consecutive mating seasons (07/08 and 08/09). I collected focal animal (>800 hours) and ad libitum data from 16 Assamese macaque females living in a wild, fully habituated group consisting of 50-60 individuals. Furthermore, I collected more than 2300 fecal samples in order to describe ovarian cycle and pregnancy characteristics and to assess the timing of ovulations and conceptions using enzyme immuneassays (EIA) for estrogen, progestogen and androgen metabolites. Endo crine profiles revealed that non-invasive monitoring of female reproductive state is feasible in Assamese macaques. Patterns of fecal androgen excretion during gestation may allow for early pregnancy detection and prenatal sex determination. Gestation length and interbirth interval fell into the range of closely related species. Females were anovulatory during the non-mating season and mostly conceived during their first ovulatory cycle within the 4-month mating season, with 65% of conceptions confined to December and January. The small subcaudal sexual swellings did not signal ovulation probability, and females lacked copulation calls and signs of behavioral estrus all of which indicate that fertility is undisclosed to males in this species. Accordingly, the long sexual consortships by high-ranking males were not linked to female fertile phases. Females exhibited extreme extended sexuality and mated throughout the mating season including acyclic and pregnant stages. Female fertile phases were randomly distributed, but the occurrence of a female s receptivity was significantly associated with the proportion of other females mating on a given day, offering a potential proximate explanation for the patterning and maintenance of extended sexuality in this and presumably other species. In addition, and in contrast to numerous non-human primate species, females did not concentrate paternities to high-ranking males but expressed non-dominance based mating biases, i.e. they mated repeatedly with a primary partner despite exhibiting high rates of promiscuity. Overall, these results suggest that in response to constraints of reproductive and life-history traits, female Assamese macaques modify and emancipate their sexual behavior from hormonal control, and thereby manipulate and control largely mating and reproductive outcome. In conclusion, this PhD-project not only gathered initial information on reproductive parameters and life-history traits for the seasonally breeding and rarely studied Assamese macaque but also contributes to the growing body of knowledge that endeavors to understand reproductive strategies of female vertebrates, sheds new light on the plasticity of female sexual behavior, and contributes to a refinement of our concept of intersexual conflict over paternity in primates.