Sexual swelling in bonobos: variations, ovulation predictability, and male responses

In most mammals, female sexual receptivity (estrus) closely coincides with ovulation, providing males with precise fertility signals. However, in some anthropoid primates living in multi-male societies, females display extended receptivity along with exaggerated sexual swellings that probabilistically indicate ovulation. This raises the question about how males successfully time mating, particularly when ovulation is difficult to predict from such cues as seen in bonobos. To address this question, we combined daily variation in swelling size, hormonal profiles, and male mating behaviors. By estimating day-specific ovulation probabilities relative to the onset of the maximal swelling phase and detumescence, we also examined how male efforts correlate with female fertility. Our results revealed that while ovulation probability was widely distributed and difficult to predict when aligned with the onset of the swelling phase, male behavior was closely aligned with the conception probability. Males concentrated mating efforts late in the phase and stopped after detumescence. High-ranking males intervened in copulations involving females with higher conception probabilities, specifically those with maximal swelling and older infants. When multiple females exhibited maximal swelling, males preferentially followed females whose maximal swelling started earlier and who had older infants. Male-male aggression increased when there were more females with maximal swelling. However, this tendency was reversed when male party size exceeded the average. Importantly, our results revealed that the low predictability of ovulation is best explained by inter- and intra-individual variation in the length of maximal swelling phase, rather than ovulation occurring randomly within that phase in bonobos. Males effectively manage such a noisy signal by prioritizing late-phase ovulatory cues and integrating reproductive history, thereby extracting usable timing information. This behavioral mechanism helps explain the persistence of conspicuous yet noisy ovulatory signals in bonobos. Since males are capable of inferring ovulation timing even under noisy conditions, selection may not favor highly precise female signals. Instead, it shifts more of the time and energy costs onto males, allowing conspicuous female traits to be maintained.