Claudia Fichtel

The evolutionary origin of human hyper-cooperation

Proactive, that is, unsolicited, prosociality is a key component of our hyper-cooperation, which in turn has enabled the emergence of various uniquely human traits, including complex cognition, morality and cumulative culture and technology. However, the evolutionary foundation of the human prosocial sentiment remains poorly understood, largely because primate data from numerous, often incommensurable testing paradigms do not provide an adequate basis for formal tests of the various functional hypotheses. We therefore present the results of standardized prosociality experiments in 24 groups of 15 primate species, including humans. Extensive allomaternal care is by far the best predictor of interspecific variation in proactive prosociality. Proactive prosocial motivations therefore systematically arise whenever selection favours the evolution of cooperative breeding. Because the human data fit this general primate pattern, the adoption of cooperative breeding by our hominin ancestors also provides the most parsimonious explanation for the origin of human hyper-cooperation.

ON THE VOCAL EXPRESSION OF EMOTION. A MULTI-PARAMETRIC ANALYSIS OF DIFFERENT STATES OF AVERSION IN THE SQUIRREL MONKEY

There is general agreement that in non-human primates, the emotional state of a caller is reflected in the vocal structure. But only few studies describe call features characterizing such correlates. This is mainly due to the fact that it is difficult to identify the emotional state of a caller. In the present study, we analysed calls from a study (Jurgens, 1979) in which squirrel monkeys had been given the opportunity to control vocalization-eliciting brain stimulation. In this way, the aversive or hedonistic quality of the emotional state underlying the production of specific calls could be determined. 758 of the recorded calls, representing 8 different call types, given by 25 subjects, were analysed in order to find out whether differences in the degree of aversion are reflected by specific acoustic parameters. It was found that an increase in aversion is parallelled, depending upon the call type, by an upward shift of maximal energy in the power spectrum, an increase in frequency range and/or an increase in the ratio of nonharmonic to harmonic energy.

Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi)

Studies in anthropoid primates and other mammals suggest that reproductive season, rank, reproductive skew, aggression received, and social support are the major factors influencing glucocorticoid output. In which way these are also affecting adrenal function in lemurid primates has been studied rarely. Here, we examine the influence of reproductive season and rank on glucocorticoid output in male sifakas (Propithecus verreauxi), a species characterized by high breeding seasonality, a hierarchy among males and extreme reproductive skew towards dominant males. We established a fecal assay for non-invasively monitoring adrenal activity and collected 315 fecal samples during the reproductive and birth season from 10 male sifakas living in 5 groups in Western Madagascar. We found a significant effect of season on glucocorticoid output, with males exhibiting higher fecal glucocorticoid levels during the reproductive compared to the birth season in conjunction with an increase in overall aggression rates during the former period. Moreover, our data indicate a significant effect of rank on adrenocortical activity with dominant males exhibiting higher glucocorticoid levels than subordinate males in the reproductive season. However, dominant males did not differ significantly in rates of initiated or received aggression and rates of affiliative behavior from subordinates but showed significantly lower rates of submission. Given their highly formalized dominance relationships, we conclude that higher glucocorticoid output in dominant males during the 4-month reproductive season is likely related to higher energetic demands necessary to cope with the challenges of male reproduction rather than to physical demands of increased fighting frequency to maintain dominance status. High rank in sifakas may thus carry high costs, which, however, may be outweighed by monopolization of almost all paternities. In sum, our data generally support the findings on the relationship between environmental and social factors and glucocorticoid output found in non-lemurid primates.

COORDINATION OF GROUP MOVEMENTS IN WILD VERREAUX'S SIFAKAS (PROPITHECUS VERREAUXI)

Summary Maintenance of group cohesion is of vital importance for group-living species. Individuals therefore need to coordinate their potentially divergent interests to maintain group cohesion. We studied behavioural aspects and mechanisms of coordinated group movements in Verreaux’s sifakas (Propithecus verreauxi), an arboreal Malagasy primate living in small groups. During a field study in Kirindy forest, western Madagascar, we studied the initiation and course of group movements, as well as vocalisations used in this context, in three social groups. We found that both sexes initiated group movements, but females did so more often, lead groups further and enlisted more followers than males. Sex of the leader had no effect on the probability that a group would feed or rest after a successful movement, however. Grumble vocalisations were emitted by both leaders and followers at high rates, both before and during group progressions, but Grumbles uttered just before an individual moved were characterised by a significantly steeper frequency modulation at the beginning of the call and higher call frequencies in both females and males. The results of this study indicated that sifakas, which evolved group-living independently from other primates, converge with many other group-living primates in several fundamental proximate aspects of group coordination and cohesion. In contrast to many other primates, however, sifakas did not use a particular call or other signals to initiate or control group movements.

A 15-Year Perspective on the Social Organization and Life History of Sifaka in Kirindy Forest

In this chapter, we summarize some fundamental demographic and morphometric data from the first 15 years of a long-term study of Verreaux’s sifaka (Propithecus verreauxi) at Kirindy Forest in Western Madagascar. We first describe this research site, its history, and infrastructure, as well as the methods employed to study a local sifaka population. Regular censuses, behavioral observations, and systematic captures of members of up to 11 groups began in 1995 and yielded a data set on demography and life history that can contribute comparative insights about sifaka life history. Our analyses revealed that average group size fluctuated very little around a mean of six individuals across years. Group composition was modified by dispersal (mostly male transfers) or disappearances, births, and deaths. Predation and female transfer were the main mechanisms triggering group extinctions and foundation of new groups (N=5 cases in 149 group years). These exceptional cases of female transfer were most likely motivated by female competition or inbreeding avoidance. One female was a member of at least four different groups. Median age at first birth was 5 years. All females gave birth to single infants, but the proportion of adult females reproducing varied between 25 and 85% across years. The mean interval between 112 births was 15.1 months. Loss of an infant before weaning reduced the subsequent inter-birth interval only by about 1 month. The probability that individual females reproduced successfully decreased as the number of adult females per group increased, implying that subtle forms of female competition limit group size. Mortality is especially high (62%) in the first 2 years of life. Predation by the fossa (Cryptoprocta ferox) is the main cause of death. Maximum female reproductive lifespan is at least 15 years, but longevity is still impossible to estimate. These analyses revealed new insights into female reproductive strategies and their interaction with social organization that were only possible because of the long-term nature of the study, but problems of small sample size still limit the analysis of many vital statistics.

Reciprocal recognition of sifaka (Propithecus verreauxi verreauxi) and redfronted lemur (Eulemur fulvus rufus) alarm calls

Redfronted lemurs (Eulemur fulvus rufus) and Verreauxs sifakas (Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls for raptors and general alarm calls for carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, even though the two species rarely interact. In a crossed design, redfronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons (Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, the two lemur species have an understanding of each others aerial as well as general alarm calls, suggesting that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.

Social networks in primates: smart and tolerant species have more efficient networks

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.

Sex-biased survival predicts adult sex ratio variation in wild birds

Adult sex ratio (ASR) is a central concept in population demography and breeding system evolution, and has implications for population viability and biodiversity conservation. ASR exhibits immense interspecific variation in wild populations, although the causes of this variation have remained elusive. Using phylogenetic analyses of 187 avian species from 59 families, we show that neither hatching sex ratios nor fledging sex ratios correlate with ASR. However, sex-biased adult mortality is a significant predictor of ASR, and this relationship is robust to 100 alternative phylogenetic hypotheses, and potential ecological and life-history confounds. A significant component of adult mortality bias is sexual selection acting on males, whereas increased reproductive output predicts higher mortality in females. These results provide the most comprehensive insights into ASR variation to date, and suggest that ASR is an outcome of selective processes operating differentially on adult males and females. Therefore, revealing the causes of ASR variation in wild populations is essential for understanding breeding systems and population dynamics.

Wild redfronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques.

Recent research has claimed that traditions are not a unique feature of human culture, but that they can be found in animal societies as well. However, the origins of traditions in animals studied in the wild are still poorly understood. To contribute comparative data to begin filling this gap, we conducted a social diffusion experiment with four groups of wild redfronted lemurs (Eulemur rufifrons). We used a ‘two-option’ feeding box, where these Malagasy primates could either pull or push a door to get access to a fruit reward to study whether and how these two behavioural traits spread through the groups. During a pre-training phase, two groups were presented with boxes in which one technique was blocked, whereas two groups were presented with unblocked boxes. During a subsequent unconstrained phase, all four groups were confronted with unblocked boxes. Nearly half of the study animals were able to learn the new feeding skill and individuals who observed others needed fewer unsuccessful task manipulations until their first successful action. Animals in the two groups with pre-training also discovered the corresponding alternative technique but preferred the seeded technique. Interestingly, animals in the two groups without pre-training discovered both techniques, and one group developed a group preference for one technique whereas the other did not. In all groups, some animals also scrounged food rewards. In conclusion, redfronted lemurs appear to use social information in acquiring a novel task, and animals in at least in one group without training developed a group preference for one technique, indicating that they have the potential to develop behavioural traditions and conformity.