Christof Neumann

Genetic Architecture of Tameness in a Rat Model of Animal Domestication

A common feature of domestic animals is tameness—i.e., they tolerate and are unafraid of human presence and handling. To gain insight into the genetic basis of tameness and aggression, we studied an intercross between two lines of rats (Rattus norvegicus) selected over >60 generations for increased tameness and increased aggression against humans, respectively. We measured 45 traits, including tameness and aggression, anxiety-related traits, organ weights, and levels of serum components in >700 rats from an intercross population. Using 201 genetic markers, we identified two significant quantitative trait loci (QTL) for tameness. These loci overlap with QTL for adrenal gland weight and for anxiety-related traits and are part of a five-locus epistatic network influencing tameness. An additional QTL influences the occurrence of white coat spots, but shows no significant effect on tameness. The loci described here are important starting points for finding the genes that cause tameness in these rats and potentially in domestic animals in general.

Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species

Compared to other mammals, sexual signals occur particularly often within the primate order. Nevertheless, little is known so far about the pressures under which these signals evolved. We studied loud calls in wild crested macaques to examine whether these are used as a sexual signal, particularly as a signal of dominance, in this species. Since the structure of loud calls may be influenced by the context in which they are uttered, we tested for contextual differences in call structure. Only males uttered loud calls and analysis of 194 loud calls given by 15 males showed that call structure encoded the callers identity as well as his social status. Dominance rank was also reflected in the frequency with which males called with alpha males calling most often. The structure of loud calls, however, was not influenced by context. Our findings consolidate the assumption that, in crested macaques, loud calls serve as a signal of dominance, most probably used to prevent contests between males for mates. We herewith provide the first direct evidence for a signal of dominance in a tolerant primate species and discuss why this signal occurs in only one sex.

Information content of female copulation calls in wild long-tailed macaques (Macaca fascicularis)

Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the females fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.

Kin-based cultural transmission of tool use in wild chimpanzees

The acquisition of a novel tool behavior to drink water spreads culturally through families in wild chimpanzees. Current research on animal culture has focused strongly on cataloging the diversity of socially transmitted behaviors and on the social learning mechanisms that sustain their spread. Comparably less is known about the persistence of cultural behavior following innovation in groups of wild animals. We present observational data and a field experiment designed to address this question in a wild chimpanzee community, capitalizing on a novel tool behavior, moss-sponging, which appeared naturally in the community in 2011. We found that, 3 years later, moss-sponging was still present in the individuals that acquired the behavior shortly after its emergence and that it had spread further to other community members. Our field experiment suggests that this secondary radiation and consolidation of moss-sponging is the result of transmission through matrilines, in contrast to the previously documented, association-based spread among the initial cohort. We conclude that the spread of cultural behavior in wild chimpanzees follows a sequential structure of initial proximity-based, horizontal transmission, followed by kin-based vertical transmission.

Complex patterns of signalling to convey different social goals of sex in bonobos, Pan paniscus

Sexual behaviour in bonobos (Pan paniscus) functions beyond mere reproduction to mediate social interactions and relationships. In this study, we assessed the signalling behaviour in relation to four social goals of sex in this species: appeasement after conflict, tension reduction, social bonding and reproduction. Overall, sexual behaviour was strongly decoupled from its ancestral reproductive function with habitual use in the social domain, which was accompanied by a corresponding complexity in communication behaviour. We found that signalling behaviour varied systematically depending on the initiator’s goals and gender. Although all gestures and vocalisations were part of the species-typical communication repertoire, they were often combined and produced flexibly. Generally, gestures and multi-modal combinations were more flexibly used to communicate a goal than vocalisations. There was no clear relation between signalling behaviour and success of sexual initiations, suggesting that communication was primarily used to indicate the signaller’s intention, and not to influence a recipient’s willingness to interact sexually. We discuss these findings in light of the larger question of what may have caused, in humans, the evolutionary transition from primate-like communication to language.

Bonobos modify communication signals according to recipient familiarity

Human and nonhuman primate communication differs in various ways. In particular, humans base communicative efforts on mutual knowledge and conventions shared between interlocutors. In this study, we experimentally tested whether bonobos (Pan paniscus), a close relative to humans, are able to take into account the familiarity, i.e. the shared interaction history, when communicating with a human partner. In five experimental conditions we found that subjects took the recipients’ attentional state and their own communicative effectiveness into account by adjusting signal production accordingly. More importantly, in case of communicative failure, subjects repeated previously successful signals more often with a familiar than unfamiliar recipient, with whom they had no previous interactions, and elaborated by switching to new signals more with the unfamiliar than the familiar one, similar to what has previously been found in two year-old children. We discuss these findings in relation to the human capacity to establish common ground between interlocutors, a crucial aspect of human cooperative communication.

Travel fosters tool use in wild chimpanzees

Ecological variation influences the appearance and maintenance of tool use in animals, either due to necessity or opportunity, but little is known about the relative importance of these two factors. Here, we combined long-term behavioural data on feeding and travelling with six years of field experiments in a wild chimpanzee community. In the experiments, subjects engaged with natural logs, which contained energetically valuable honey that was only accessible through tool use. Engagement with the experiment was highest after periods of low fruit availability involving more travel between food patches, while instances of actual tool-using were significantly influenced by prior travel effort only. Additionally, combining data from the main chimpanzee study communities across Africa supported this result, insofar as groups with larger travel efforts had larger tool repertoires. Travel thus appears to foster tool use in wild chimpanzees and may also have been a driving force in early hominin technological evolution. DOI: http://dx.doi.org/10.7554/eLife.16371.001

Degrees of freedom in social bonds of crested macaque females

Social bonds between group members affect individual fitness and wellbeing. While the impact of bond strength is well studied, the consequences of bond predictability and equitability are often overlooked. Similarly, whether bonds reflect short-term contingencies and/or long-term social strategies remains understudied. We investigated these questions in female crested macaques, Macaca nigra, which display a tolerant social style within a nepotistic hierarchical social structure. We analysed the structure of social bonds by testing whether similarity within dyads (in kinship, dominance and age) predicted the strength, predictability and equitability of bonds. We then tested the value of social bonds by analysing the effect of their characteristics on three fitness-related behaviours: coalitionary support, feeding-in-proximity and aggression. We found that the bond characteristics of females differed substantially from those of other species with comparable data: bonds were of average strength, of moderate endurance and relatively balanced. Stronger bonds were more equitable but less predictable than weaker bonds. Closely ranked females, but not kin or age peers, had stronger, more predictable and more equitable bonds than others. Coalitionary support was not related to any of the bond characteristics, feeding-in-proximity was positively associated with strength and predictability and aggression was positively linked to strength and negatively to equitability. These results highlight the complex picture of the benefits of social bonds in this species. They reflect the degrees of freedom tolerant macaque females can express in their social relationships within their stable social structure, a pattern that may not be given enough consideration in stable nepotistic hierarchical societies. Comparative research is necessary to establish whether these patterns are more general than previously thought or a specific feature of tolerant macaques. Investigating various characteristics of bonds together is paramount to appreciate the dynamics of social relationships and to better understand the social components of fitness.

Contextual encoding in titi monkey alarm call sequences

Many primates produce one type of alarm call to a broad range of events, usually terrestrial predators and non-predatory situations, which raises questions about whether primate alarm calls should be considered ‘functionally referential’. A recent example is black-fronted titi monkeys, Callicebus nigrifrons, which emit sequences of B-calls to terrestrial predators or when moving towards or near the ground. In this study, we reassess the context specificity of these utterances, focussing both on their acoustic and sequential structure. We found that B-calls could be differentiated into context-specific acoustic variants (terrestrial predators vs. ground-related movements) and that call sequences to predators had a more regular sequential structure than ground-related sequences. Overall, these findings suggest that the acoustic and temporal structure of titi monkey call sequences discriminate between predator and non-predatory events, fulfilling the production criterion of functional reference.Significance statementPrimate terrestrial alarm calls are at the centre of an ongoing debate about meaning in animal signals. Primates regularly emit one alarm call type to ground predators but often also to various non-predatory events, raising questions about the referential nature of these signals. In this study, we report observational and experimental data from wild titi monkeys and show that terrestrial alarm calls are usually given in sequences of acoustically distinct variants composed in structurally distinct ways depending on the external event. These differences are salient and could help recipients to distinguish the nature of the call eliciting event. Since most previous studies on animal alarm calls have not checked for acoustic variants within different call classes, it may be premature to conclude that primate terrestrial calls do not meet the criteria of functional reference.

Female chimpanzees adjust copulation calls according to reproductive status and level of female competition

Female chimpanzees, Pan troglodytes, are usually depicted as sexually submissive and bound by male coercion, because males are able to monopolize oestrous females, limiting a females options for mate choice. We present behavioural data from a group of wild chimpanzees during a rare period in which up to 10 females cycled simultaneously, which prevented males from monopolizing oestrous females, thus changing the dynamic of male-female sexual interactions. Overall, we found that nulliparous and parous females employed different copulation calling strategies, reflecting their relative reproductive attractiveness and social standing within the community. Male partner rank, copulation duration and dominant male audience further influenced calling behaviour, and there was a nonsignificant trend for females to increase calling as the number of cycling females increased. We conclude that female chimpanzees are capable of adjusting their copulation calling flexibly, by taking into account their own sexual attractiveness, to incite male competition.