Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalizeafter copulation, but the function of these vocalizations isnot clear. In this article, we examine the hypothesis that copulationcalls are a form of postcopulatory female choice. Accordingto this hypothesis, copulation calls are honest signals of fertility(i.e., ovulation) that are used by females to encourage mateguarding by their preferred mating partners and reduce the likelihoodof sperm competition. Evidence in favor of this hypothesis isreviewed and discussed in relation to other hypotheses. We suggestthat the evolution of female copulation calls in primates islinked to the evolution of other female mating signals suchas exaggerated sexual swellings, the potential for sperm competition,and the opportunity for precopulatory female mate choice.     

Structure and use of distance calls in wild bonobos (Pan paniscus)

We report the physical structure and use of a distance call (high-hoot) by wild bonobos (Pan paniscus).Although spectrographic analyses reveal high structural variability, the total sample can be subdivided according to the composition of units—the presence or absence of an initial segment—and the range of the lowest harmonic. Analyses of samples from male—female pairs,vocalizing simultaneously and in close proximity, reveal that both animals utter calls in more or less precise temporal alternation but with different spectral ranges. Whether these differences are gender-specific or related to other factors, such as age or the social relations between particular individuals, is not clear. We suggest that (a) individuals of the same party may coordinate their vocal activity on both the temporal and the spectral level and (b) high hootings stimulate emission of equal vocalizations by members of other parties and may increase cohesion among community members. Comparison of a restricted number of spectrograms from known individuals indicates that bonobos may be able to adjust spectral parameters of one type of distance calls (high- hoot) according to corresponding calls of conspecifics.     

Information content of female copulation calls in yellow baboons.

In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.     

Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome

In a number of primate species, females utter loud and distinctive calls during mating. Here we aim to clarify the information content and function of Barbary macaque (Macaca sylvanus) copulation calls by testing (i) whether or not copulation calls advertise the female fertile phase and (ii) whether and how copulation calls influence male ejaculatory behaviour. In order to do this, we combined hormone measurements with acoustic analysis and behavioural observations. In contrast to a previous study implying that the structure of copulation calls indicates the timing of the fertile phase, our results, using objective endocrine criteria for assessing ovulation, provide evidence that the structure of copulation calls of female Barbary macaques does not reveal the timing of the fertile phase. More importantly, females seem to influence the likelihood of ejaculation by calling versus remaining silent and by adjusting the timing of call onset. Females make use of this ability to influence mating outcome to ensure ejaculatory matings with almost all males in the group. In addition, calls given during ejaculatory copulations differ from those during non-ejaculatory copulations, providing information about mating outcome for listeners. We conclude that in this species, copulation calls apparently serve to enhance sperm competition and maximize paternity confusion.     

Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas (Theropithecus gelada) to compare with published accounts of social knowledge in chacma baboons (Papio ursinus). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male''s response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.     

Parasites physically block host copulation: a potent mechanism of parasite-mediated sexual selection

Research on the role of parasites in sexual selection has focusedmainly on host mate choice favoring relatively unparasitizedmales. But parasites can also generate variance in host reproductivesuccess by influencing the ability of individual hosts to directlycompete among themselves for mates or fertilizations, a subjectarea that has received far less attention. We demonstrate experimentallythat parasitism by mites can drive sexual selection by way ofa novel mechanism involving male competition: physical inhibitionof host copulation. Mite resistance in natural populations isheritable, emphasizing the evolutionary potential of parasite-mediatedsexual selection in this system and indicating that femalesshould be receiving indirect fitness benefits as a result ofthis process. We show that parasitism by mites, Macrochelessubbadius, reduces mating success of male Drosophila nigrospiracula.Smaller males were more strongly compromised, identifying hostbody size as a tolerance trait. As parasite load increased,the rate at which males attempted to copulate but failed becauseof obstruction by mites increased. When mites were removed frominfested males, host mating success was restored. Thus, thephysical presence of the mites per se generates differentialmating success, in this case by interrupting the normal flowof mating behaviors. This study elucidates a potent mechanismof parasite-mediated sexual selection in a system wherein parasiteresistance is demonstrably heritable, and as such expands ourunderstanding of the evolutionary potential of sexual selection.     

Extended phenotypes as signals

Animal signals may result from construction behaviour and can provide receivers with essential information in various contexts. Here we explore the potential benefits of extended phenotypes with a signalling function as compared to bodily ornaments and behavioural displays. Their independence of the body, their physical persistence and the morphological and cognitive conditions required for their construction allow unique communication possibilities. We classify various levels of information transfer by extended phenotype signals and explore the differences between secreted signals and signals resulting from collection and construction, which usually involve higher behavioural complexity. We examine evolutionary pathways of extended phenotypes with a signalling function with help of a comparative evaluation and conclude that often constructions first provide a direct fitness benefit, with a signalling function becoming more and more prominent during evolutionary progression. The abundance and variability of extended phenotypes as signals is impressive and provides unique possibilities for animal communication research.     

Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

Sexual conflict as a partitioning of selection

Sexual conflict appears to be a powerful force in evolution. We suggest that selection theory can readily be adapted for cases of sexual conflict and illustrate how it can provide a new perspective on what traits cause conflict and might respond to its presence. Use of selection theory resolves some terminological confusion, provides operational measures of conflict and generates a conceptual tool for parsing the causes and consequences of conflict in complex systems of male–female interactions.     

Female competition and aggression: interdisciplinary perspectives

This paper introduces a Theme Issue combining interdisciplinary perspectives in the study of female competition and aggression. Despite a history of being largely overlooked, evidence is now accumulating for the widespread evolutionary significance of female competition. Here, we provide a synthesis of contributions to this Theme Issue on humans and other vertebrates, and highlight directions for future research. Females compete for resources needed to survive and reproduce, and for preferred mates. Although female aggression takes diverse forms, under most circumstances relatively low-risk competitive strategies are favoured, most probably due to constraints of offspring production and care. In social species, dominance relationships and threats of punishment can resolve social conflict without resort to direct aggression, and coalitions or alliances may reduce risk of retaliation. Consistent with these trends, indirect aggression is a low cost but effective form of competition among young women. Costs are also minimized by flexibility in expression of competitive traits, with aggressive behaviour and competitive signalling tailored to social and ecological conditions. Future research on female competition and the proximate mediators of female aggression will be greatly enhanced by opportunities for interdisciplinary exchange, as evidenced by contributions to this Theme Issue.     

Monogamy,strongly bonded groups,and the evolution of human social structure

Human social evolution has most often been treated in a piecemeal fashion, with studies focusing on the evolution of specific components of human society such as pair‐bonding, cooperative hunting, male provisioning, grandmothering, cooperative breeding, food sharing, male competition, male violence, sexual coercion, territoriality, and between‐group conflicts. Evolutionary models about any one of those components are usually concerned with two categories of questions, one relating to the origins of the component and the other to its impact on the evolution of human cognition and social life. Remarkably few studies have been concerned with the evolution of the entity that integrates all components, the human social system itself. That social system has as its core feature human social structure, which I define here as the common denominator of all human societies in terms of group composition, mating system, residence patterns, and kinship structures. The paucity of information on the evolution of human social structure poses substantial problems because that information is useful, if not essential, to assess both the origins and impact of any particular aspect of human society.     

Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird

Across diverse taxa, morphological traits mediate social interactions and mate selection. Physiological constraints on signal elaboration have been widely documented, but the potential for trait display to influence physiological state remains poorly understood. We tested for the presence of causal links between ventral plumage colour—a trait known to covary with reproductive performance—and physiological measures in female North American barn swallows, Hirundo rustica erythrogaster. Naturally darker swallows have lower levels of plasma oxidative damage. Females manipulated to display darker ventral plumage during reproduction rapidly decreased oxidative damage, adopting the physiological state of naturally darker individuals. These results support the presence of a social mechanism that links static plumage traits with the physiological state of their bearer during trait advertisement, long after the completion of signal development.     

The social organizations of squirrel monkeys: Implications for ecological models of social evolution

“Squirrel-monkeys occur in a considerable number of slightly different forms, but all are built upon a similar body plan and have a basic color scheme. One of the larger races—from inner Perú—is also the most colorful and one of the brightest colored of all mammals. It may be taken as a point of departure. The top of the head and the upper and outer parts of the body and the upper side of the basal half of the tail are a vivid green, with a pepper and salt effect of yellow and gray. The face is pure white except for black spectacles, muzzle and chin; the throat, chest, underside, insides of limbs, and the underside of the basal half of the tail are brilliant daffodil yellow. The terminal half of the tail is jet black and rather bushy. The flesh of the hands is pale pink. Other races vary in the intensity of the green and yellow, so that some may be olive brown above and white below, and in the amount and arrangement of the black areas on the face and the tip of the tail. Some have almost naked ears, others have these organs clothed in short fur, and still others bear thereupon long tufts or fringes. All these variations seem to blend into the other geographically . . . some of these pure color variations may constitute valid regional subspecies or even species. . . .” I. T. Sanderson¹ (p. 77).     

Agent-based modelling as scientific method: a case study analysing primate social behaviour

A scientific methodology in general should provide two things: first, a means of explanation and, second, a mechanism for improving that explanation. Agent-based modelling (ABM) is a method that facilitates exploring the collective effects of individual action selection. The explanatory force of the model is the extent to which an observed meta-level phenomenon can be accounted for by the behaviour of its micro-level actors. This article demonstrates that this methodology can be applied to the biological sciences; agent-based models, like any other scientific hypotheses, can be tested, critiqued, generalized or specified. We review the state of the art for ABM as a methodology for biology and then present a case study based on the most widely published agent-based model in the biological sciences: Hemelrijk's DomWorld, a model of primate social behaviour. Our analysis shows some significant discrepancies between this model and the behaviour of the macaques, the genus used for our analysis. We also demonstrate that the model is not fragile: its other results are still valid and can be extended to compensate for these problems. This robustness is a standard advantage of experiment-based artificial intelligence modelling techniques over analytic modelling.     

The evolution of social philopatry in female primates

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.