Male and female reproductive strategies in relation to paternity outcome in Barbary macaques

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From an evolutionary point of view, differential reproduction is the most important aspect of life, because it is the central focus of natural selection. An animal’s reproductive strategy determines its contribution to the species’ gene pool, and is hence an important variable on which natural selection operates. The theory of sexual selection predicts that competition for mates between individuals of the same sex (typically males), and mate choice (typically by females) drives the evolution of certain traits (e.g. large body size and canine size, bright colors, ornaments, horns, sex skin swellings). The reason why sexual selection might be biased towards inter-male competition and female choice was later explained in terms of an asymmetry in parental investment. Males produce a large number of sperm cells and thus can potentially have a high number of offspring, in which they usually invest little. Since male reproductive success is limited by the number of successfully fertilized females, males should compete for access to as many fertile females as possible to maximize their reproductive success. Females, on the other hand, produce only few egg cells and are more limited in their number of offspring than males, while often investing far more energy in begetting and raising their young than do males. Therefore females should carefully select their mates and actively solicit those males who meet their needs in order to enhance the fitness of their offspring and thereby their own reproductive success. Given the different strategies that males and females follow to maximize their reproductive success, it is obvious that there is a conflict between the sexes over reproduction. In most species, however, the role of male and female strategies and the interplay between these roles in determining an individual’s reproductive success is poorly understood.
Among primates, sexual selection has for a long time been envisioned as operating principally among males and primate mating systems have thus usually been described as being male dominated or controlled. In species living in multimale-multifemale groups, both sexes are likely to affect paternity outcome, but the different selective forces operating on male and female reproductive processes can be expected to lead to opposing strategies (see above). Male dominance, and thereby the ability to monopolize access to fertile females, seems to be one of the main factors influencing a male’s lifetime reproductive success in many primate species. However, nowadays there is increasing evidence that other factors (e.g. alternative mating strategies, post-copulatory mechanisms) are also involved, and that female primates are not only passive recipients of “male choice”, but do show preferences for certain males as mating partners and might thus play an important role in paternity determination. However, information on the relative importance of male and female reproductive strategies upon paternity outcome in primates is still limited.
To study the mechanisms leading to paternity and to examine the relative importance of male and females in determining male reproductive success, the Barbary macaque is a particularly interesting species due to the following characteristics: i) highly seasonal breeding with a potentially high degree of overlap between fertile phases providing females with more freedom to escape male monopolization attempts, ii) an almost equal adult sex ratio, with the consequence that many males compete with each other for access to fertile females, iii) an apparently low degree of male-male aggression and a less strict dominance hierarchy, iv) extended consortships do not occur, suggesting that males have little opportunity to monopolize access to fertile females, v) a highly promiscuous mating system, with females often being observed to actively solicit males and to mate with multiple males in rapid succession. All these characteristics suggest that male contest competition over females is low and that therefore in Barbary macaques the females might have a relatively high influence on paternity outcome, different to the situation seen in many other macaque species.
Studies on reproductive success in this species so far have led to contradicting results. In contrast to a study on a semi-free ranging population in which a clear relation between rank and reproductive success was found, a recent study on the Gibraltar population showed no clear relationship between rank and paternity. Furthermore, no study has yet investigated the proximate mechanisms underlying paternity outcome in this species, irrespective of whether paternity is related to male rank or not. Hence, it remains unclear to what extent the reproductive strategies of males and females interact and what the relative contributions of these strategies are for determining paternity outcome in the Barbary macaque.
The overall aim of this thesis was therefore to examine the relative importance of male and female reproductive strategies in determining paternity outcome in a free-ranging group of Barbary macaques in Gibraltar in order to contribute to a better understanding of the proximate mechanisms regulating reproductive success in multimale-multifemale primate groups. The study combined detailed behavioral observations on sexual activity with non-invasive methodologies for the assessment of female reproductive status and determination of paternity based on fecal analysis.
In an initial step (chapter 2) information on the distribution of mating activity throughout the ovarian cycle, particularly in relation to the timing of ovulation was examined. For this, a combination of behavioral observation and endocrinological data from 13 free-ranging
Chapter 5: Summary
females gathered over a period of four mating seasons was used. Data on i) rates of copulation (ejaculatory, non-ejaculatory), ii) patterns of male inspections of females and iii) time spent in consortship were related to the time of ovulation and the female fertile phase in order to clarify if males do concentrate their mating effort around ovulation and whether or not timing of the fertile phase in Barbary macaques is concealed from males. In addition, the data were related to female sex hormone levels. The results indicated that all behaviors varied predictably with ovarian cycle stage. Rates of copulations were found to increase towards the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. There was also a significant cycle phase effect on the proportion of time spent in consortship and inspection rate with values being significantly higher during the fertile phase compared to the pre- and postfertile phase for consortships and between the fertile and postfertile phase for male inspections. Frequencies of all three male sexual behaviors were significantly correlated with levels of female sex hormones, with rates of ejaculatory copulations and proportion of time spent in consortship being highly positively correlated with female estrogen levels. In sum, this part of the study provided clear evidence that despite a high degree of female promiscuity, Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Moreover, the results suggested that estrogen related cues are involved in the process of recognition of female reproductive status by males, which provided the basis for studying the nature of these cues.
It was therefore investigated on which cue(s) males might make their mating decision (chapter 3). Specifically, the value of anogenital swelling and female sexual behavior (cues that have been shown to be estrogen related in other primate species) in advertising female fertility status, and the relative role they may play as a signal to males used for timing their reproductive effort (e.g. ejaculatory copulations), was investigated. Data on anogenital swelling size, using digital images, and copulatory behavior of 11 females were collected during four mating seasons and data on female sexual behavior were collected during two of the four seasons. The data were related to the time of ovulation and the fertile phase. Specifically it was investigated i) how frequencies of female sexual behaviors and anogenital swelling size change throughout the ovarian cycle and in particular in relation to the timing of ovulation, ii) whether rates of female sexual behaviors and swelling size are elevated during the fertile phase compared to the pre- and postfertile phase of the female cycle iii) whether rates of male copulations (ejaculatory and non-ejaculatory) differ between stages of maximum and pre- and post-maximum swelling size and iv) whether and in which way female sexual behaviors and the size of the swelling are related to female estrogen levels. Overall, rates of all female sexual behaviors examined were not correlated with female estrogen levels and did not significantly differ between the fertile and non-fertile phases of the cycle. In contrast, swelling size was significantly correlated with female estrogen levels and increased predictably towards ovulation, with size being maximal during the fertile phase. Moreover, frequencies of male ejaculatory copulations showed a strong positive correlation with swelling size and highest rates were found during maximum swelling. The results provide strong evidence that female Barbary macaques honestly signal the probability of fertility through sexual swelling and that males apparently use this information to time their mating activities. This should in principle then facilitate male monopolization behavior. On the other hand, as mentioned before, female Barbary macaques should have a high degree of freedom to exert direct mate choice.
The final question pursued in chapter 4 was therefore to examine what actually determines paternity outcome in the Barbary macaque. Specifically the relative importance of male monopolization, female direct mate choice and postcopulatory mechanisms in influencing male reproductive success were examined using a combination of behavioral observations, endocrine assessment of the female fertile phase, and paternity determination from 8 females, collected over a period of two mating seasons. Paternity outcome, number and duration of consortships, female sexual behaviors and copulations were analyzed to investigate i) how paternity is distributed between high- and low-ranking males, ii) whether there are rank-related differences in male consortship behavior and male mating success, iii) whether the frequencies of female proceptive and receptive behaviors differ in relation to male rank and iv) if the assigned fathers differ from non-fathers with respect to consortship behavior, mating success, and solicitations and mating refusals received from females. The majority of infants of which paternity was determined, were sired by high-ranking males. The results indicated that this rank-related reproductive skew was not due to successful male monopolization, since females were only half of the observation time during their fertile phase consorted by males. More importantly, females were in consort with at least two different males during the fertile phase. High-ranking males, however, consorted females significantly more often and for a longer duration compared to low-ranking males and also showed significantly higher rates of copulation and ejaculation. In addition, there was a rank-related difference in female solicitation frequencies, with a strong bias towards high-ranking males. The frequencies/duration of behaviors shown by or towards the assigned fathers, however, did not significantly differ from those shown by or towards non-fathers. Collectively, the data
Chapter 5: Summary
indicate that rank is an important determinant of male reproductive success in free-ranging Barbary macaques. More importantly, however, they suggest that the observed reproductive skew between males is related more to mechanisms of female direct mate choice than to male monopolization of fertile females. Since, however, females mated with many males and fathers were not preferred over non-fathers, paternity seemed to be determined by mechanisms operating at the post-copulatory level, such as sperm competition or cryptic female choice.
Taken together, by combining behavioral, endocrinological and genetic data, this thesis has contributed new information to a better understanding of the proximate mechanisms influencing male reproductive success in free-ranging Barbary macaques. The data clearly suggest that Barbary macaque males are able to discern the female fertile phase based on an honest signal provided by the female which, given the data available, seems to be a common feature among macaque species. Although this helps males to concentrate copulations to the time when conception probability is high, male monopolization was not an important determinant of male reproductive success. Female direct mate choice and post-copulatory mechanisms rather seem to be the predominant determinants of male reproductive success in the Barbary macaque. Mating promiscuously but concentrating paternity in dominant males, may help female Barbary macaques to receive a number of benefits (e.g. receiving “good sperm”, avoiding genetic incompatibilities, reducing the risk of infanticide). However, further studies on these potential benefits and their possible fitness consequences for males and females are needed. This will improve our understanding of how sexual selection has shaped the reproductive biology of the Barbary macaque and, more generally, would also contribute to a better understanding of the evolution and behavioral ecology of primates.