Faculty of Biology and Psychology, Georg-August University School of Science (GAUSS), 37077 Göttingen, GERMANY.
In promiscuous mating systems, several males compete with each other for access to fertile females, and males have evolved a variety of mating tactics to outcompete their rivals. Mate-guarding is a mating tactic used by males of several vertebrate and invertebrate taxa to exclude other males from accessing the guarded female, and hence secure their paternity. In multi-male mammal groups, high- ranking males are often the ones mate-guarding females the most, since they gain priority of access to females and are the only one capable of efficiently monopolising females. Whereas mate-guarding has been proven to increase male reproductive success, this mating tactic may also entail some costs associated with life-history trade-offs between current and future reproduction, body condition maintenance and survival. In turn, these costs may limit the ability of top-ranking males to monopolise females and hence affect male reproductive skew (i.e. the partitioning of reproduction among males). Costs of mating tactics may also promote the evolution of male mate-choice by forcing the males to concentrate their reproductive effort on the females with the highest fitness value. Quantifying the costs of mate-guarding may therefore shed light on the factors driving the evolution of male mating decisions and ultimately contributes to our understanding of variation in male reproductive skew.
Primates are an interesting taxa to study this question since several species live in stable multi-male groups and mate-guarding is a highly beneficial mating tactic commonly employed by high-ranking males. However, studies investigating the costs of mate-guarding in primates are mainly limited to the quantification of feeding costs and yielded, so far, inconsistent results. Our understanding of these costs is also impaired by the lack of a reliable non-invasive physiological marker of energetic condition in non-hominid primates.
The overall aim of this thesis was therefore to quantify the costs of mate-guarding for males in a primate species living in multi-male groups, the long-tailed macaques (Macaca fascicularis). In this species, alpha males mate-guard females to a lower extent than predicted by the Priority of Access model, suggesting that costs of mate-guarding may limit males’ ability to monopolise females. In study 1, I evaluated the suitability of urinary C-peptide (UCP, a by-product of insulin production) as a marker of male energetic status in macaques. In study 2 and 3, I quantified the energetic, physiological and physical (i.e. aggression) costs of mate-guarding. Finally, in study 4, I investigated the influence of female value on the costs of mate-guarding and the investment of males into this behaviour.
To carry out the validation of UCP as a reliable marker of energetic status in non-hominid primates (study 1), I first investigated the relationship between UCP measures and indexes of body condition in free-ranging and captive macaques. UCP levels were positively correlated with body-mass index and skinfold-fatness across individuals. In addition, a food reduction experiment revealed that UCP levels co-varied with changes in both body mass and dietary intake. UCP is therefore a useful marker to track non-invasively intra- and inter-individual variations in body condition and nutritional status.
Subsequently, I studied, during two mating periods, three groups of wild long-tailed macaques living in the Ketambe research area, Gunung Leuser National Park, Indonesia. To provide a comprehensive picture of the potential costs of mate-guarding, while controlling for environmental factors, I combined 1) focal behavioural observations on males’ activity, height in the canopy, and socio-sexual interactions, 2) GPS records of distance travelled, 3) non-invasive measurements of physiological stress levels (faecal glucocorticoids, fGC) and energetic status (UCP) and 4) assessments of fruit availability. In total 2088 hours of focal data, 331 urine samples and 771 faecal samples were collected and analysed and 360 fruit trees were surveyed monthly.
In study 2, I found that mate-guarding reduced parameters of both energy intake and expenditure but had no significant overall effect on a male’s energetic status (UCP levels). These results suggest that energy intake and expenditure were balanced during mate-guarding in the study males.
Study 3 revealed that during mate-guarding, males had, in general, higher fGC levels but this effect was modulated by a male’s vigilance time. Mate-guarding also increased a male’s vigilance time and male-male aggression rates. In addition, alpha males were more stressed than other males year round, independently of mating competition. I suggest that elevated glucocorticoid levels during mate-guarding may help males to maintain their energetic homeostasis but may constitute a long- term cost inherent to the risk of exposure to chronic stress. The combination of this physiological cost and the risk of injury associated with aggression may limit the ability of alpha males to mate- guard females and hence affect male reproductive skew.
In study 4, I showed that male long-tailed macaques may reduce some costs of mate-guarding by selectively monopolising females with high reproductive value since males had lower fGC when mate-guarding high-ranking parous females. Furthermore, males adjusted their mate-guarding investment to female quality by being more vigilant and more aggressive when mate-guarding high ranking females or females with whom they had stronger bonds. This later result shows that males make mate-guarding choices not only by mate-guarding highly valuable females longer, but also by monopolising them better.
In this thesis I identified clear costs of mate-guarding in a primate species and highlight how these costs may influence male reproductive skew. I suggest that male long-tailed macaques may have evolved an “incomplete female monopolisation strategy” whereby males limit the costs of mate- guarding by selectively mate-guarding only certain females and by monopolising females of low value less thoroughly. This incomplete female monopoly may be a crucial component of a top-ranking male’s overall energy management strategy allowing him to respond to rank challenges year round and hence enhance the alpha tenure length and associated fitness benefits.
By comparing my results with other mammalian taxa, I discuss in this thesis how the relationship between costs of male reproductive effort and reproductive skew might be modulated by 1) reproductive seasonality, 2) male energy management strategy, 3) males’ top dominance rank achievement process and 4) social structure.
Future studies on the cost of male mating tactics should consider the complexity of male reproductive effort, which is not limited solely to the reproductive periods and may be distributed over the whole year and expressed as male-male competition for dominance status or social interactions.