Date of Award

12-1-2019

Degree Name

Doctor of Philosophy

Department

Anthropology

First Advisor

Reichard, Ulrich

Abstract

Among multi-male, multi-female primate groups, males engage in direct contest competition for access to mates. The priority-of-access model (PoA model) generally predicts that male reproductive success increases with male dominance rank, but the strength of this relationship is expected to decrease with increasing female reproductive synchrony, particularly in seasonally breeding primates. Genetic paternity studies support the model’s predictions, having found a positive relationship between male dominance rank and reproductive success. However, in addition to dominance status and female reproductive synchrony, a number of proximate factors also impact males’ ability to sire offspring, which have not been considered in studies of male reproductive strategies.By integrating behavioral, genetic, morphological, and hormonal analysis as more direct measures of reproductive success in individual males, this dissertation investigated the relationship between male dominance rank and reproductive success and including the proximate factors affecting this relationship in wild northern pig-tailed macaques (Macaca leonina). The main objectives of this study are: 1) to identify the relationships between male dominance rank, male mating success, and male reproductive success, and assess to what extent female synchrony affects these relationships; 2) to identify the proximate factors that may reduce the reproductive success of the top-ranking male and assess variation in male mating tactics related to dominance rank and migration status (i.e., resident males vs. extra-group males); and 3) to evaluate the function of males’ red ornaments that may be used to signal male dominance status (male-male competition) to attract females (female mate choice) or both. The study was conducted at Khao Yai National Park, northeastern Thailand. Systematic data collection on CH group occurred from September 2015-June 2017. The group composition was recorded daily as well as births, deaths, individual emigrations and immigrations, females’ parity status, and the presence of extra-group males (EGMs). Sociosexual data and male-female interactions (i.e., copulations, ejaculatory copulations, consortships, grooming, female proceptive behaviors and receptive behaviors) were recorded during females’ receptive periods. To assess male reproductive success, genetic paternity analyses were conducted on fecal DNA samples collected from 18 adult and subadult males, 22 adult females, and 25 juveniles and infants. To measure red skin coloration of males, hindquarter images were collected non-invasively for seven adult males. From those images, skin color and luminance were computationally quantified to assess variation in male anogenital reflectance. Lastly, fecal samples were collected from nine adult males to assess monthly levels of fecal testosterone by microtitreplate enzyme immunoassay. The distribution of births and matings suggested that northern pig-tailed macaques, at least in this group, are best categorized as moderate seasonal breeders. Indeed, 33-67% of births occurred within a three-month period. Copulation data revealed a positive relationship between male dominance rank and mating success, supporting the predictions of the PoA model. However, the distribution of male reproductive success indicated that: 1) high-ranking males controlled a proportion of paternity much lower than predicted by the PoA model; 2) middle-ranking males controlled a proportion of paternity higher than predicted by the model; and 3) EGMs, not considered in the PoA model, controlled a surprisingly large proportion of paternity despite a low observed mating success. When females were simultaneously receptive, lower-ranking and subadult males engaged in opportunistic and surreptitious copulation and avoided direct competition with higher-ranking males, and most females approached and mated with EGMs out of the resident adult males’ sight. However, one EGM also mated in full sight of resident adult males. This is the first study to report mating and successful paternity by EGMs in a moderately seasonally breeding species.Four male mating tactics were identified: 1) the top-ranking resident male tactic, in which the male competes for the alpha male position to control priority of access to receptive females through long consortships and copulations; 2) the lower-ranking resident male tactic, in which the male copulates opportunistically and surreptitiously out of sight of higher-ranking males mostly during the mating peak; 3) the subordinate EGM tactic, in which the male lives semi-solitarily and copulates opportunistically and surreptitiously, mostly during the mating peaks; and 4) the super-dominant EGM tactic, in which the EGM copulates irrespective of the presence of other males and in full sight of even the highest-ranking resident male. In addition, I found support for female mate choice. Darker and redder males had more mating partners, received more female proceptive behaviors, and were engaged in more consortships and grooming with receptive females. Furthermore, males became redder and darker as female reproductive synchrony increased. Together, these results suggest that male red ornaments exhibited in the male’s anogenital area is attractive to females. Furthermore, behavioral evidence of female mate choice towards EGMs was found. This dissertation provides a comprehensive picture of the complex male mating tactics of northern pig-tailed macaques. To achieve reproductive success, males engage in a diversity of mating tactics, strongly influenced by male dominance rank and the degree of female reproductive synchrony. However, mate-guarding costs, surreptitious copulations by lower-ranking males and EGMs, and female mate choice, need to be included in an extended version of the PoA model to provide stronger predictions of the distribution of male reproductive success in primates.

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