Sandra Winters

Sexually selected skin colour is heritable and related to fecundity in a non-human primate

Sexual selection promotes the prevalence of heritable traits that increase an individuals reproductive rate. Despite theoretically strong directional selection, sexually selected traits can show inter-individual variation. Here, we investigate whether red skin ornamentation, a rare example of a male mammalian trait involved in mate attraction, influences fecundity and is heritable in rhesus macaques (Macaca mulatta), and explore the mechanisms that are involved in maintaining trait variation. Interestingly, the trait is expressed by and is attractive to both sexes. We collected facial images of 266 free-ranging individuals and modelled skin redness and darkness to rhesus macaque vision. We used 20 years of genetic parentage data to calculate selection gradients on the trait and perform heritability analyses. Results show that males who were both darkly coloured and high-ranking enjoyed higher fecundity. Female skin redness was positively linked to fecundity, although it remains unclear whether this influences male selectiveness. Heritability explained 10–15% of the variation in redness and darkness, and up to 30% for skin darkness when sexes are considered separately, suggesting sex-influenced inheritance. Our results suggest that inter-individual variation is maintained through condition-dependence, with an added effect of balancing selection on male skin darkness, providing rare evidence for a mammalian trait selected through inter-sexual selection.

Who cares? Experimental attention biases provide new insights into a mammalian sexual signal

The effects of intrasexual and intersexual selection on male trait evolution can be difficult to disentangle, especially based on observational data. Male-male competition can limit an observers ability to identify the effect of female mate choice independently from sexual coercion. Here, we use an experimental approach to explore whether an ornament, the red facial skin exhibited by male rhesus macaques (Macaca mulatta), might be involved in both female mate choice and male-male competition. We used a noninvasive experimental approach based on the looking time paradigm in a free-ranging setting, showing images of differently colored male faces to both adult females (N = 91) and males (N = 77), as well as to juveniles (N = 94) as a control. Results show that both adult females and males looked longer at dark red faces compared with pale pink ones. However, when considering the proportion of subjects that looked longer at dark red faces regardless of preference strength, only females showed a significant dark red bias. In contrast, juveniles did not show any preferences between stimuli, suggesting that the adult bias is not a consequence of the experimental design or related to a general sensory bias for red coloration among all age-sex classes. Collectively, these results support the role the ornament plays in female mate choice in this species and provide the first evidence that this ornament may play a role in male-male competition as well, despite a general lack of observational evidence for the latter effect to date.

Multimodal Advertisement of Pregnancy in Free-Ranging Female Japanese Macaques (Macaca fuscata)

The role of multiple sexual signals in indicating the timing of female ovulation, and discrimination of this timing by males, has been particularly well studied among primates. However the exhibition of pregnancy signals, and how such signals might modulate male post-conception mating decisions, is still poorly understood. Here we aimed to determine if Japanese macaque males use changes in female sexual signals (behavioral, visual and auditory) to discriminate pregnancy and adjust their socio-sexual behaviors. We combined behavioral observations, digital photography and endocrinological (progestogen and estrogen) data, collected systematically during three one-month periods: the pre-conceptive period, the 1st month of pregnancy and the 2nd month of pregnancy. We analyzed variation in the probability of detecting male and female socio-sexual behaviors and estrus calls, as well as changes in female face color parameters, in relation to female reproductive state. Based on our focal observations, we found that males did not copulate during the pregnancy period, and that female socio-sexual behaviors generally decreased from the pre-conceptive to post-conceptive periods. Female face luminance decreased from the pre-conceptive month to the pregnancy period whereas face color only varied between the 1st and 2nd month of gestation. Our results suggest that Japanese macaque females display sexual cues of pregnancy that males might use to reduce energy wasted on non-reproductive copulations with pregnant females. We hypothesize that females advertize their pregnancy through changes in behavioral, visual and potential auditory signals that males can use to adjust their mating behaviors. We finish by discussing implications for male and female post-conception strategies.

Dr Seuss and the real Lorax

The modern US environmental movement was born in 1970. The year began with the National Environmental Policy Act on 1 January and closed with the establishment of the Environmental Protection Agency on 2 December. Other milestones occurred in April, including the first observance of Earth Day — then the largest grassroots demonstration in history, drawing an estimated 20 million people globally1 — and the release of ‘Big Yellow Taxi’, a folksong by Joni Mitchell that quickly became the eco-anthem for the environmental movement. It was in this highly charged atmosphere that Theodor ‘Dr Seuss’ Geisel resolved to write an environmental book for children. Geisel began to set down words, not pausing to agonize over rhyming and rhythm or even to sketch characters. He noted that he had read so many “dull things on conservation, full of statistics and preachy”, that making such a subject amusing “was the hard part” and he suffered from writer’s block2. It wasn’t until months later, in September 1970, when Geisel visited the exclusive Mount Kenya Safari Club3, that a breakthrough happened: “I had nothing but a laundry list with me, and I grabbed it... I wrote 90% of [The Lorax] that afternoon”2 (Fig. 1a).

Is male rhesus macaque facial coloration under intrasexual selection

Exaggerated male traits can evolve under intra- or intersexual selection, but it remains less clear how often both mechanisms act together on trait evolution. While the males of many anthropoid primate species exhibit colorful signals that appear to be badges of status under intrasexual selection, the red facial coloration of male rhesus macaques (Macaca mulatta) appears to have evolved primarily under intersexual selection and female mate choice. Nonetheless, experiments show that red color is salient to males, raising the question of whether the signal may also be under intrasexual selection. Here, we examine whether males express this signal more strongly in competitive contexts. Facial images were collected on all 15 adult males of a free-ranging social group during the peak of the mating season, and coloration was quantified using visual models. Results show that males more similar in facial redness were more likely to interact aggressively than more dissimilar ones, suggesting that color may be involved in the assessment of rivals. Furthermore, males exhibited darker coloration on days they were observed copulating, and dominance rank predicted facial redness only on copulating days, suggesting that coloration may also advertise motivation to defend a mate. Male rhesus macaque facial coloration may thus mediate agonistic interactions with rivals during competition over reproductive opportunities, such that it is under both inter- and intrasexual selection. However, color differences were small, raising perceptibility questions. It remains possible that color variation reflects differences in male condition, which in turn alter investment towards male-male competition and mating effort.

Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.

Martin Stevens: Sensory Ecology, Behaviour, and Evolution

Sensory ecology is a relatively new field of study that focuses on the ways in which animals obtain and use information about their surroundings. Approaches based on questions of sensory perception have been increasingly integrated into primatological research, particularly in the areas of foraging and communication. In his seminal volume “Sensory Ecology,” Dusenbery (1992) focused primarily on the acquisition of information, the physical properties of signals in different sensory modalities, and the ways in which these relate to different types of behavior, especially those related to spatial navigation and migration. In Sensory Ecology, Behaviour, and Evolution, Martin Stevens sets out to integrate this sensory approach with evolutionary theory and behavioral ecology by refocusing on the evolutionary processes and adaptive significance of perception and its links to behavior. The book itself is relatively slim. Given the potential breadth of topics and wealth of examples from the literature, such a broad subject cannot be covered exhaustively in a single volume. Instead, Sensory Ecology, Behaviour, and Evolution serves as a general introduction to the topic. The book is divided into five parts: 1) Introduction, 2) Sensory Processing, 3) Communication, 4) Diversification and Divergence, and 5) Conclusions, with the bulk of the content concentrated in the middle 3 parts. Each part consists of one to four chapters that provide an overview of the theoretical issues associated with, and the empirical investigation of, different topics. Stevens has elected to structure the book not around sensory modalities (as in Dusenbury 1992), but by concepts such as sensory integration, sensory exploitation, and sensory drive. By doing so, he emphasizes how different sensory modalities can be influenced by the same evolutionary processes (albeit sometimes in different ways) and encourages readers always to consider the total sensory experience of the animal and the way in which this is influenced by and influences evolutionary adaptation. Int J Primatol (2015) 36:205–208 DOI 10.1007/s10764-015-9811-y

Primatology and conservation in Hanoi, Vietnam.

H anoi, Vietnam was host to the 25 Congress of the International Primatological Society (IPS) from August 11 to 16, 2014. A wide variety of research was presented at this conference, including studies focused on primate genetics, behavior, and communication. Organized around the theme “Meeting the Challenges of Conserving Primate Diversity,” the conference emphasized primate species endemic to Southeast Asia.

John C. Mitani, Josep Call, Peter M. Kappeler, Ryne A. Palombit, Joan B. Silk (eds): The Evolution of Primate Societies

Twenty-five years have passed since the publication of Primate Societies (Smuts et al. 1987). In that time primatology has changed a great deal in its theoretical underpinnings, its technical possibilities and methods, the nature and extent of its empirical scope, and sadly, in the status of its subjects in the wild. Intended as a follow-up synthesis of the field, The Evolution of Primate Societies aims to provide an integrated overview of the state of play in primatology. With 32 extensive chapters written by many of primatology’s most established authorities, we should start by saying that this book really is a tome, and we doff our collective caps to the editors. Putting this together was clearly no small effort, and our field owes them a great debt for their dedication and service. The book is organized in five “parts.” These represent an overview of the primate order (Part 1, titled: “Primate Behavioral Diversity”), survival and development (Part 2, titled: “Surviving and Growing Up in a Difficult and Dangerous World”), reproduction (Part 3, titled: “Mating and Rearing Offspring”), sociality (Part 4, titled: “Getting Along”), and cognition (Part 5, titled: “Cognitive Strategies for Coping with Life’s Int J Primatol (2013) 34:1298–1303 DOI 10.1007/s10764-013-9731-7