Age negatively impacts reproduction in high-ranking male rhesus macaques on Cayo Santiago, Puerto Rico

Abstract

Based on sexual selection theory, the reproductive potential of male primates is expected to be limited by access to fertile females. Alpha males, the highest ranking males in a social group, are predicted to have better access to mates and produce more offspring until they are no longer dominant, which usually corresponds with age. Little is known about male reproductive senescence independent of rank changes in nonhuman primates. Here, we examine variation in the reproductive success of high-ranking male rhesus macaques on cayo Santiago. We recorded behavioral data for 21 adult males across 9 social groups during the 2013 mating season. Additionally, we used paternity data from the long-term database to determine the number of offspring each subject sired over his lifetime and during the study period. Older high-ranking males in stable groups had fewer offspring than younger high-ranking males in stable groups in 2013. The low reproductive output for the older males was not a result of lower mating effort, and reproductive output in 2013 was not predicted by total prior reproductive success. our results provide novel evidence of post-copulatory reproductive senescence in high-ranking male nonhuman primates.

Twenty-three-year demographic history of the Affenberg Japanese macaques (Macaca fuscata), a translocated semi-free-ranging group in southern Austria

“…During the 23 years of our investigation, only four alpha males kept their alpha status until death or separation from the group for veterinary care. Stable dominance hierarchies, in terms of male social rank, are not uncommon in groups of Japanese macaques (Perloe 1992;Huffman 1991a) and are well described in other hierarchically organized species such as free-ranging rhesus macaques (Macaca mulatta; Manson 1992;Milich et al 2020) and baboons (Papio hamadryas ursinus; Beehner et al 2005).…”

“…We are aware that more data are needed to examine a possible relationship between male social rank and reproductive success in our study group. We assume, however, that the novelty-seeking nature of females and the stability of male rank hindered topranking males from maintaining high reproductive success after a certain period of being present in the group (Huffman 1991a, b, Huffman, 1992Inoue and Takenaka 2008;Perloe 1992, also see Milich et al 2020 for data on Macaca mulatta).…”

The biology of aging in a social world: insights from free-ranging rhesus macaques

“…Given that a steady decline in bone mineral density also begins at age 17, this change in bone condition may be akin to the accelerated rate of bone loss seen in perimenopausal women (Lo et al, 2011). Older males on Cayo Santiago also experience bone diseases that may be related to reproductive decline, as high-ranking males over the age of 18 sire fewer offspring than younger conspecifics, unrelated to mating effort (Milich et al, 2020). Older males also display lower fecal androgen levels than younger males during the birth season (Higham et al, 2013), and future research in the population will be useful for determining whether hormonal changes related to reproductive senescence are responsible for the skeletomuscular changes observed in older individuals.…”

Male‐philopatric nonhuman primates and their potential role in understanding the evolution of human sociality

“…For example, in a study of male rhesus macaques, older males that were high-ranking, had high lifetime reproductive success, and had high rates of mating activity during the study period had lower success rates of siring offspring that year compared to younger males, even those that did not mate as frequently, potentially suggesting either postcopulatory reproductive senescence or cryptic female choice. 143 In geladas, females terminate pregnancies after takeovers in which the dominant male in their group is replaced. 144 Similarly, in the male-philopatric hamadryas baboons, there is evidence of pregnancy termination after takeovers.…”

“…In studies of wild populations, data on reproductive effort compared to the success of siring offspring could reveal inconsistencies that point to mechanisms of cryptic female choice. For example, in a study of male rhesus macaques, older males that were high‐ranking, had high lifetime reproductive success, and had high rates of mating activity during the study period had lower success rates of siring offspring that year compared to younger males, even those that did not mate as frequently, potentially suggesting either postcopulatory reproductive senescence or cryptic female choice 143 . In geladas, females terminate pregnancies after takeovers in which the dominant male in their group is replaced 144 .…”