Female ano-genital swelling as a complex sexual signal: morphological, behavioral and hormonal correlates in wild Macaca maura (H.R. Schinz, 1825)

Abstract

Conspicuous sexual swelling is a unique morphological signal shown by some Old World primates: sexual hormones (estrogens and progestogens, which also regulate ovulation) cyclically drive the female sexual skin, tail and rump to "exaggeratedly" swell. As a signal of ovulation, it increases female attractiveness to males, granting females, beyond mere conception, likely direct (e.g., male services) and indirect (e.g., good genes) benefits. On the other hand, it should grant males accurate paternity estimates. However, given the conspicuousness, long duration, potential imprecision to pinpoint ovulation, and a potential multi-modality in the signaling display (co-occurrence of multiple signal of ovulation, i.e. morphological, behavioral and/or chemical cues) swelling reliability seems to be doubtful, at least in some species. In fact, according to the graded signal hypothesis, sexual swelling is a graded and probabilistic signal of ovulation, for which the best competitor male will tend to monopolize females only at peak swelling, obtaining the high probability to sire offspring whereas, lower ranking males will tend to mate outside peak swelling, having a lower (but not zero) chance to fertilize the female. Female would benefit from paring with dominant male at peak swelling (“biasing paternity”), obtaining likely direct and indirect benefits; however, by mating with multiple partners (“confusing paternity”), female faces a lower infanticide risk. Other than benefits, sexual swelling has also been suggested to encompass some energetic costs, especially due to its conspicuousness and cyclical renewal: e.g., a likely increased body weight might affect behavioral activities; water retention involved in the production of swelling might affect water requirements; it increases male-male competition and, likely, harassment rate towards females. We explored morphological, behavioral and hormonal correlates of sexual swelling in the endangered moor macaque (Macaca Maura; South Sulawesi, Indonesia), in order to investigate: (i) sexual swelling signaling, and (ii) likely energetic costs that females have to face during this part of the ovulatory cycle. As for the first aim, we investigated the gradual increase of sexual swelling according to size categories (small, medium, large), and tested the reliability of the signal to advertise ovulation, by analyzing estrogen/progestogen metabolites; we then explored a likely multi-modal signaling (female proceptive behavior and chemical cues); finally, we tested male response and his ability to detect ovulation. As for the second aim, we investigated potential energetic costs that fully swollen females (large swelling) may face by comparing them with females during (a) a potentially low cost energetic state (cycling/not swollen) and (b) a potentially high cost energetic state (lactating). We compared activity budget, nutrient/water/energy intake, nutritional status (by C-peptide analysis), and physiological stress levels (by fecal glucocorticoid metabolite, FGCM, analysis). Ecological constraints such as seasonality (wet/dry season) and food availability (phonological data) have been taken into account, as well as harassment rate by males towards females. We found that sexual swelling is a graded and - on average - reliable signal of ovulation and that males conveyed their mating effort when swelling is maximum. We also found that proceptive behavior gradually increases with swelling size, suggesting a likely multi-modality in advertising ovulation. In this respect, data supported the hypothesis that sexual swelling may serve both male and female in biasing paternity; nonetheless, the overlap in duration among swellings of different females, the long plateau duration (signal is maximum for about 9 days), and consortships with multiple partners (up to 3) observed throughout a single plateau, further suggested that sexual swelling may also serve females confusing paternity, according to the graded signal hypothesis. As for the energetics, we found that, while lactating females showed behavioral strategies aimed at increasing feeding, nutrient and energy inputs - as a likely strategy to balance out the energetic cost of lactation – fully swollen females did not (and no differences were found for C-peptide levels among female groups). Fully swollen females rather redirected their time towards interactions with males experiencing a severe decrease of nutrient/energy intake. It appears that fully swollen female sexual imperative overcame that for food intake in a "play all out" strategy. Furthermore, the female water intake and the time spent eating fruits (a watery item) increase when water availability increases (wet season), might then be interpreted as a likely strategy to balance physiological water needs of swelling edema. In addition, fully swollen females experienced a higher aggression rate than in any other phase of the cycle. Body energetic distress, water metabolism and social stressors may all contribute to the higher FGCM levels in fully swollen females, than cycling/not swollen females, suggesting sexual swelling phase to encompass energetic costs for M. maura reproduction.