Abstract
BackgroundFemale signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females’ interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour.ResultsWe show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this.ConclusionThough probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.
Highlights
Female signals of fertility have evolved in diverse taxa
The general framework of the socio-ecological model postulates that females distribute themselves in space with respect to food resources, and that males distribute themselves with respect to the distribution of males [10,11,12]. These factors create the selective environment in which females evolve to indicate oestrus to males with increasing or decreasing accuracy, and the distribution of females in space and time determines the general likelihood that females will exhibit sexual swellings [8]
Unlike in many previous studies of other primate species, where sexual swellings but not behaviour indicated the timing of ovulation [e.g. Barbary macaques, 14; olive baboons, [15,24]], or where behaviour but not sexual swellings indicated ovulation [e.g. long-tailed macaques, [17]], measures of both sexual swelling size and sexual behaviour indicated intra-cycle variation in fertility, potentially indicating the timing of ovulation to males
Summary
Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. One prevailing model for the evolution of these signals is the gradedsignal hypothesis, which proposes that swellings represent probabilistic signals of intra-cycle variation in fertility, with swellings being largest when this probability is highest, and smallest when it is lowest, such that ovulation occurs during the maximal swelling period [8]. This model proposes that such probabilistic signals exist in multi-male multi-female groups both to confuse and assure males of paternity. By biasing paternity towards good quality males, females may obtain a variety of indirect and direct benefits, while still enabling sufficient paternity confusion to prevent infanticide from other males who are unlikely (but not impossible) to be fathers
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
