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Southern Illinois University Carbondale OpenSIUC Dissertations Theses and Dissertations 12-1-2019 MALE REPRODUCTIVE STRATEGIES IN WILD NORTHERN PIG- TAILED MACAQUES (MACACA LEONINA): TESTING THE PRIORITY-OF-ACCESS MODEL Florian (Allen Trebouet Southern Illinois University Carbondale, [email protected] Follow this and additional works at: https://opensiuc.lib.siu.edu/dissertations Recommended Citation Trebouet, Florian (Allen, "MALE REPRODUCTIVE STRATEGIES IN WILD NORTHERN PIG-TAILED MACAQUES (MACACA LEONINA): TESTING THE PRIORITY-OF-ACCESS MODEL" (2019). Dissertations. 1765. https://opensiuc.lib.siu.edu/dissertations/1765 This Open Access Dissertation is brought to you for free and open access by the Theses and Dissertations at OpenSIUC. It has been accepted for inclusion in Dissertations by an authorized administrator of OpenSIUC. For more information, please contact [email protected]. MALE REPRODUCTIVE STRATEGIES IN WILD NORTHERN PIG-TAILED MACAQUES (MACACA LEONINA): TESTING THE PRIORITY-OF-ACCESS MODEL by Florian Trébouet M.S., Bordeaux Sciences Agro, 2011 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Doctor of Philosophy degree Department of Anthropology in the Graduate School Southern Illinois University Carbondale December 2019 DISSERTATION APPROVAL MALE REPRODUCTIVE STRATEGIES IN WILD NORTHERN PIG-TAILED MACAQUES (MACACA LEONINA): TESTING THE PRIORITY-OF-ACCESS MODEL by Florian Trébouet A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the field of Anthropology Approved by: Dr. Ulrich H. Reichard, Chair Dr. Gretchen R. Dabbs Dr. Susan M. Ford Dr. Dario Maestripieri Dr. Suchinda Malaivijitnond Dr. Jeremiah E. Scott Graduate School Southern Illinois University Carbondale May 6, 2019 AN ABSTRACT OF THE DISSERTATION OF Florian Trébouet, for the Doctor of Philosophy degree in Anthropology, presented on May 6, 2019, at Southern Illinois University Carbondale. TITLE: MALE REPRODUCTIVE STRATEGIES IN WILD NORTHERN PIG-TAILED MACAQUES (MACACA LEONINA): TESTING THE PRIORITY-OF-ACCESS MODEL MAJOR PROFESSOR: Dr. Ulrich H. Reichard 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 i 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 ii 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 iii 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. iv ACKNOWLEDGMENTS I am deeply indebted to my dissertation advisor, Dr. Ulrich Reichard, for all of his valuable advice, assistance, and encouragement throughout my doctoral journey. Without him, I would have never been able to reach this goal. Besides my advisor, I would also like to thank the rest of my dissertation committee members—Dr. Suchinda Malaivijitnond, Dr. Susan Ford, Dr. Jeremiah Scott, Dr. Dario Maestripieri, and Dr. Gretchen Dabbs—for their great support and insightful guidance throughout the different stages of my dissertation. I would like to express my deepest appreciation to Dr. Malaivijitnond for all of her invaluable contribution, helpful advice, and indefinite support, especially during my field research when I needed most. She was the first person to introduce me to the wonderful world of primatology in 2009. She has been by my side since then and will hopefully be so for many more years. I would also like to extend my deepest gratitude to Dr. Ford for all of her insightful guidance and moral support. I am extremely grateful to my outstanding field assistants—Chris Coll-Beswick, Corey Bither, Michelle Reed, and Nik Long—for their invaluable help and hard work in collecting all the data that have contributed to this dissertation. I am thankful for their extreme patience and kindness. This dissertation would have never been possible without them. I am also appreciative of all the remarkable people of Khao Yai National Park, Thailand—Jambee,
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