James P. Higham

Baboon sexual swellings: Information content of size and color

Primate sexual swellings are hormone-dependent sexual signals that play a key role in determining patterns of behavior. They are among the most conspicuous signals exhibited by any mammal, and their large size and bright coloration have fascinated evolutionary biologists for well over a century. A number of different adaptive hypotheses have been proposed for the evolution of sexual swellings, and there have been several recent attempts to test some of these using precise swelling measurements made in the field. Most of these studies have focused only on the size element of the swelling, and those that have measured other aspects of swellings, such as color, have done so only crudely. A focus solely on swelling size is inconsistent with most theoretical models of mate choice, which emphasize the importance of multiple cues within sexual signals. Here, we present data on baboon (Papio hamadryas anubis) sexual swellings, including measures of both swelling size and color, measured objectively using digital photography at Gashaka-Gumti National Park, Nigeria. We combined these measurements with detailed data on fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period around ovulation based on those levels. We show that swelling color and size vary independently, and that, consistent with results in other species, swelling size contains information about the timing of ovulation and the fertile period. However, we show that swelling color does not contain such information. In addition, swelling size contains information about female parity, and we found some evidence to suggest that color may also contain such information. These results indicate that baboon sexual swellings may contain information about multiple aspects of female fertility. We discuss the implications of these results for understanding the nature of swellings as behavioral signals, and the role of swellings in mate choice.

Studying Primate Color: Towards Visual System-dependent Methods

Primates exhibit a striking diversity of colors and patterns in their pelage and skin markings, used in functions as diverse as camouflage to sexual signaling. In studying primate colors, it is important to adopt approaches not based on human assessment wherever possible, and that preferably take account of the visual system of the appropriate receiver(s). Here, we outline some of the main techniques for recording the colors exhibited and encountered by primates, including the use of digital photography and reflectance spectrometry. We go on to discuss the main approaches for analyzing the data obtained, including those not linked to a particular visual system, such as direct analyses of reflectance spectra. We argue that researchers should strive for analyses based on the visual system of the relevant receiver, and outline some of the main modeling approaches that can be used, such as color space and discrimination threshold modeling. By analyzing color measures with respect to specific visual systems, field studies can link behavioral ecology to the visual and cognitive sciences, and move toward descriptions of signal information content that incorporate elements of receiver psychology. This in turn should lead to a greater understanding of the detection and interpretation of signals by receivers, and hence their likely use in decision making.

An introduction to multimodal communication

Though it has long been known that animal communication is complex, recent years have seen growing interest in understanding the extent to which animals give multicomponent signals in multiple modalities, and how the different types of information extracted by receivers are interpreted and integrated in animal decision-making. This interest has culminated in the production of the present special issue on multimodal communication, which features both theoretical and empirical studies from leading researchers in the field. Reviews, comparative analyses, and species-specific empirical studies include manuscripts on taxa as diverse as spiders, primates, birds, lizards, frogs, and humans. The present manuscript serves as both an introduction to this special issue, as well as an introduction to multimodal communication more generally. We discuss the history of the study of complexity in animal communication, issues relating to defining and classifying multimodal signals, and particular issues to consider with multimodal (as opposed to multicomponent unimodal) communication. We go on to discuss the current state of the field, and outline the contributions contained within the issue. We finish by discussing future avenues for research, in particular emphasizing that ‘multimodal’ is more than just ‘bimodal’, and that more integrative frameworks are needed that incorporate more elements of efficacy, such as receiver sensory ecology and the environment.

The energetics of male–male endurance rivalry in free-ranging rhesus macaques, Macaca mulatta

In many animal species, males engage in endurance rivalry, competing for mating opportunites over extended durations. In the rhesus macaque, a seasonally breeding primate species, energetically costly mating behaviours such as consortship lead to greater reproductive success, and the ability of males to improve their body condition before the mating season may be crucial in determining their ability to use such strategies. Here, we explore relationships between male dominance rank, behaviour, body mass index (BMI) and energetics (assessed through urinary C-peptide of insulin levels, UCPs) in free-ranging rhesus macaques during a 6-month birth season and subsequent 6-month mating season. We analysed measures of general activity, mating behaviours and restlessness, here defined as the rate of change between behaviours. During the birth season, high-ranking males spent more time feeding on high-energy food, were less restless and spent less time travelling than low-ranking males. Restlessness and travelling time were both negatively correlated with male BMI and UCPs. Males in good condition during the birth season were in good condition at the onset of the mating season. During the mating season, high-ranking males participated in more consortships, which were positively correlated with copulatory activity. Copulation was negatively correlated with UCP levels, demonstrating the cost of such mating activities. As a consequence, by the end of the mating season, high-ranking males were in the worst condition. Our results suggest that male rhesus macaques engage in competitive endurance rivalry, and that male condition built during the previous birth season is an integral part of mating success.

Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques

Animals signal their reproductive status in a range of sensory modalities. Highly social animals, such as primates, have access not only to such signals, but also to prior experience of other group members. Whether this experience affects how animals interpret reproductive signals is unknown. Here, we explore whether familiarity with a specific female affects a males ability to assess that females reproductive signals. We used a preferential looking procedure to assess signal discrimination in free-ranging rhesus macaques, a species in which female facial luminance covaries with reproductive status. We collected images of female faces throughout the reproductive cycle, and using faecal hormone analysis to determine ovulation, categorized images as coming from a females pre-fertile, ovulating, or post-fertile period. We printed colour-calibrated stimuli of these faces, reproducing stimuli perceptually the same in colour and luminance to the original appearance of females. These images were presented to males who were either unfamiliar or familiar with stimuli females. Overall, males distinguished ovulatory from pre-ovulatory faces. However, a significant proportion of males did so only among males familiar with stimuli females. These experiments demonstrate that familiarity may increase a receivers ability to use a social partners signals to discern their reproductive status.

Mu-opioid Receptor (OPRM1) Variation, Oxytocin Levels and Maternal Attachment in Free-Ranging Rhesus Macaques Macaca mulatta

Understanding the genetic and neuroendocrine basis of the mother-infant bond is critical to understanding mammalian affiliation and attachment. Functionally similar nonsynonymous mu-opioid receptor (OPRM1) SNPs have arisen and been maintained in humans (A118G) and rhesus macaques Macaca mulatta (C77G). In rhesus macaques, variation in OPRM1 predicts individual differences in infant affiliation for mothers. Specifically, infants carrying the G allele show increased distress on separation from their mothers, and spend more time with them upon reunion, than individuals homozygous for the C allele. In humans, individuals possessing the G allele report higher perceptions of emotional pain on receiving rejection by social partners. We studied maternal behavior over the course of a year among free-ranging female rhesus macaques on Cayo Santiago, Puerto Rico. We then trapped females and collected blood samples from which we assessed OPRM1 genotype; we also collected cerebrospinal fluid samples from which we measured oxytocin (OT) levels. We show that females possessing the G allele restrain their infants more (i.e., prevent infants from separating from them by pulling them back) than females homozygous for the C allele. Females possessing the G allele also show higher OT levels when lactating, and lower OT levels when neither lactating nor pregnant, than females homozygous for the C allele. This is the first study to demonstrate an association between OPRM1 genotype and maternal attachment for infants, and is one of the first studies of any free-ranging primate population to link functional genetic variation to behavior via potentially related neuroendocrine mechanisms.

Sexual signalling in female crested macaques and the evolution of primate fertility signals

BackgroundFemale signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females’ interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour.ResultsWe show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this.ConclusionThough probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.

Dominance, Coloration, and Social and Sexual Behavior in Male Drills Mandrillus leucophaeus

Sexual selection has driven the evolution and elaboration of a wide variety of displays and ornaments in male nonhuman primates, including capes, cheek flanges, and sexual coloration. Among the most sexually dimorphic of all primates is the drill (Mandrillus leucophaeus), the males of which can be 3 times the mass of females, possess large canines, and exhibit extremely bright sexual skin coloration. However, the function of male coloration in this species has never been examined. Here, we present data on male color (measured objectively using digital photography), dominance rank, measures of male-female association, and key sexual behaviors, of adult male drills (n = 17) living in four semi free-ranging enclosures at the Drill Rehabilitation and Breeding Center in Nigeria. We test the hypothesis that male coloration is a badge of status, indicating dominance rank, and the hypothesis that male coloration attracts females. We found that male coloration did indicate rank, and that high ranking, strongly colored males were more likely to associate with adult females, and more specifically with fully tumescent females. These males also engaged in more sexual activity. However, measures of male-female association and sexual behaviors were not related to male color once rank had been taken into consideration; i.e., for males of a given rank, females did not prefer those that were more colorful. We discuss the results in light of what is known about the wild drill social system, in which unfamiliar individuals may come together in “supergroups,” and in which quality indicators of competitive ability may be particularly important.

The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons

Baboon researchers commonly use the timing of sexual swelling detumescence to infer the timing of ovulation. These estimates are then used for a variety of purposes, including the interpretation of male and female behaviour, assessment of likely paternity, and the calculation of gestation lengths. Although captive studies have measured the timing of ovulation with respect to detumescence, this has not been measured in wild baboons. Here, we use observational data on female sexual swellings, and hormonal data measured from faeces, to investigate the timing of ovulation with respect to detumescence in wild olive baboons. Our data show similar variability in the timing of ovulation with respect to detumescence as that produced by captive studies, although there are some notable differences, including the absence of any ovulations measured on or after the day of swelling detumescence. We discuss the importance of our results for baboon researchers using swellings to infer ovulation as part of their studies.

Primate brain size is predicted by diet but not sociality

The social brain hypothesis posits that social complexity is the primary driver of primate cognitive complexity, and that social pressures ultimately led to the evolution of the large human brain. Although this idea has been supported by studies indicating positive relationships between relative brain and/or neocortex size and group size, reported effects of different social and mating systems are highly conflicting. Here, we use a much larger sample of primates, more recent phylogenies, and updated statistical techniques, to show that brain size is predicted by diet, rather than multiple measures of sociality, after controlling for body size and phylogeny. Specifically, frugivores exhibit larger brains than folivores. Our results call into question the current emphasis on social rather than ecological explanations for the evolution of large brains in primates and evoke a range of ecological and developmental hypotheses centred on frugivory, including spatial information storage, extractive foraging and overcoming metabolic constraints.