Female Chimpanzees Use Copulation Calls Flexibly to Prevent Social Competition

Citation: Townsend SW, Deschner T, Zuberb uhler K ( Female Chimpanzees Use Copulation Calls Flexibly to Prevent Social Competition Simon W. Townsend 0 Tobias Deschner 0 Klaus Zuberbu hler 0 David Reby, University of Sussex, United Kingdom 0 1 School of Psychology, University of St Andrews , St Andrews, Scotland , United Kingdom , 2 Budongo Conservation Field Station, Masindi , Uganda , 3 Max Planck Institute for Evolutionary Anthropology , Leipzig , Germany The adaptive function of copulation calls in female primates has been debated for years. One influential idea is that copulation calls are a sexually selected trait, which enables females to advertise their receptive state to males. Male-male competition ensues and females benefit by getting better mating partners and higher quality offspring. We analysed the copulation calling behaviour of wild female chimpanzees (Pan troglodytes schweinfurthii) at Budongo Forest, Uganda, but found no support for the male-male competition hypothesis. Hormone analysis showed that the calling behaviour of copulating females was unrelated to their fertile period and likelihood of conception. Instead, females called significantly more while with high-ranking males, but suppressed their calls if high-ranking females were nearby. Copulation calling may therefore be one potential strategy employed by female chimpanzees to advertise receptivity to high-ranked males, confuse paternity and secure future support from these socially important individuals. Competition between females can be dangerously high in wild chimpanzees, and our results indicate that females use their copulation calls strategically to minimise the risks associated with such competition. - Funding: This study has been funded by a studentship provided by the Biotechnology and Biological Sciences Research Council of the United Kingdom to ST in addition to BBSRC BB/D002559/1 and EU Pathfinder FP-6 What it means to be human grants to KZ. Hormone analysis was funded through the German Max Planck Society. The Budongo Forest Project receives core funding from the Royal Zoological Society of Scotland. The funders did not have a role in study design, data collection and analysis, decision to publish, or preparation of manuscript. Competing Interests: The authors have declared that no competing interests exist. In various animal species copulations are accompanied by a distinct vocal behaviour, the copulation call (e.g. African elephants (Loxodonta africana) [1], lions (Panthera leo) [2], elephant seals (Mirounga angustirostris) [3], and humans (Homo sapiens) [4]). Due to their prevalence, considerable debate has surrounded the adaptive significance of these conspicuous acoustic signals. In primates, copulation calls are loud, acoustically distinctive vocalisations emitted prior to, during or just after copulation. Calls can be produced by both males and females participating in the copulation, however in Old World monkeys and apes, it is more commonly females that vocalise [57]. Interestingly, not all copulations are accompanied by calling behaviour, suggesting that females have some control over call production. A number of different hypotheses have been put forward to explain the adaptive significance of copulation calls [7], although it is unlikely that any one hypothesis in isolation is sufficient to explain call evolution. Indeed, copulation calls may operate at more than one level with multiple functions [8]. The most common hypothesis invoked to account for the evolution of such calls is that they are sexually selected traits to alert males, other than the mating partner, to the receptive condition of the female caller [3,5,6,811], with the result of inciting competition amongst them. The incitation of male-male competition hypothesis [3] can operate at two distinct levels, which are not mutually exclusive [12]. Firstly, calls may operate to stimulate overt competitive interactions between males so that, indirectly, the female ends up with the most dominant partner [13]. Copulations accompanied by a call are predicted to primarily occur with low-ranking, less desirable males and increase subsequent levels of male aggression. Aggressive interactions can also occur during or after copulation to prevent insemination or future matings [9]. Secondly, copulation calls may lead to multiple mating partners, and this could generate additional benefits for the female due to sperm competition [10]. Under this scenario, males do not attempt to prevent insemination per se, but they should be particularly motivated to mate with the female shortly after a successful mating by another male. If female calling behaviour has been shaped by sperm competition, females should call to advertise ejaculation [10] and calling should decrease the interval between successive matings [8]. Polyandrous mating, and sperm competition that follows from it, increases paternity confusion for individual males, and it has been argued that this lowers the risk of male infanticide [10]. In contrast to the male-male competition hypothesis, however, the paternity confusion hypothesis makes no predictions about females trying to increase the quality of partners or sperm. Instead, females are primarily interested in receiving copulations from as many socially important partners as possible, safeguarding them from their infanticidal tendencies and gaining their future support. In many primate species females are notoriously vulnerable to infanticide [14,15], suggesting that there are strong selective pressures acting on females to evolve behavioural or sexual counter-strategies to protect their infants: copulation calls may well be one such counterstrategy. Although the theoretical reasoning behind the incitement of male-male competition and the paternity-confusion hypotheses is sound, the desired empirical support is weak, especially for chimpanzees. Most empirical work so far has been done with different monkey species, which are typically matrilineally bonded [8,10,13,1618], in contrast to male-bonded chimpanzees. A second relevant point is that if copulation calls function to increase a females reproductive success, or confuse paternity amongst multiple males, then it is reasonable to predict that callers should take into account (a) at which stage in their cycle they are (b) whether the desired mating partners are present in the audience. A number of studies have investigated the influence of the female reproductive stage on vocal production. For example femalealpine accentors, Prunella collaris, sing only during their fertile time-period [19] and the stereotyped 50kHz vocalisations produced by female brown rats are only given during pro-oestrus [20]. In primates, it has also been suggested that copulation calls change based on female sexual status [10,12], but hormonal data are not usually available to determine the precise time of ovulation. Very little is known about the degree to which female p (...truncated)