Female behavioral proceptivity functions as a probabilistic signal of fertility, not female quality, in a New World primate

Abstract

The interests of males and females in mating contexts often conflict, and identifying the information conveyed by sexual signals is central to understanding how signalers manage such conflicts. Research into the information provided by female primate sexual signals has focused on exaggerated anogenital swellings as either reliable-indicators of reproductive quality (reliable-indicator hypothesis) or probabilistic signals of fertility (graded-signal hypothesis). While these morphological signals are mostly confined to catarrhine primates, these hypotheses are potentially widely applicable across primates, but have not been tested in taxa that lack such morphological signals. Here, we tested these hypotheses in wild black capuchins (Sapajus nigritus), a species in which females lack morphological sexual signals but produce conspicuous behavioral estrous displays. Specifically, we examined the proportion of time different females spent producing these signals with respect to measures of female quality (dominance rank, parity, age-related fecundity and cycle type) and in relation to the timing of fertility, as determined by analysis of fecal progesterone. Time spent displaying did not vary across females based on measures of female quality, but increased with the approach of ovulation. Further, male mating effort varied according to the timing of female fertility. Proceptive behaviors in this species thus meet predictions of the graded-signal hypothesis, providing the first support for this hypothesis based solely on behavioral signals.

Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals

“…Our results suggest that both of these phenotypes enable the extraction of meaningful skin colour variation, although it is known that other various factors, including olfactory, haptic, behavioural and auditory signals, may also play important roles in sexual behaviour in female platyrrhines [47–49]. The improvement of accuracy through sessions for training pairs in protanopia, deuteranopia and LMS-even trichromacy (figure 2 a ), and the lack of this effect for test pairs (figure 2 b ), may reflect participant learning the correct images of training faces according to feedback in the absence of other reliable clues.…”

Assessing female reproductive status of spectral tarsier (Tarsius tarsier) using fecal steroid hormone metabolite analysis

“…Fecal samples were lyophilized, pulverized, and extracted with 80% methanol in water as described by Heistermann, Tari, and Hodges (). Extracts were analyzed in the Endocrinology Laboratory of the German Primate Center for concentrations of progesterone and estrogen metabolites using enzyme immunoassays (EIA) for the measurement of 5α‐reduced‐20‐oxo pregnanes (5‐P‐3OH) and total estrogens (E‐total), which both have previously been applied successfully to monitor female ovarian activity and pregnancy in numerous species of primates (e.g., Barelli, Heistermann, Boesch, & Reichard, ; Higham et al, ; Möhle, Heistermann, Dittami, Reinberg, & Hodges, ; Ostner & Heistermann, ; Tiddi, Wheeler, & Heistermann, ). For 5‐P‐3OH measurements, fecal extracts were diluted 1:500 to 1:4,800 (depending on concentration) with assay buffer (0.04M PBS, pH 7.2) before being measured by EIA as described by Dehnhard et al ().…”

Do sexual calls in female black capuchin monkeys (Sapajus nigritus) vary with fertility? An acoustic analysis

“…However, while the rate of production of the visual components of the proceptive displays have been demonstrated to be a probabilistic signal of ovulation to males (i.e. proceptive displays gradually increase in frequency with the approach of ovulation), the rate of production of noncopulatory sexual calls did not raise accordingly with the approach of ovulation (Tiddi et al, 2015). It remains unclear, however, whether their acoustic structure could change in relation to the timing of ovulation, thus potentially providing listeners with information about the timing of the female fertile phase.…”

“…Robust (or tufted) capuchin monkeys (genus Sapajus) represent an ideal study system to explore the adaptive significance of sexual calls because females in this genus signal sexual proceptivity via a rich repertoire of visual sexual signals, as well as through distinct vocalizations uttered almost exclusively around the period of female behavioral proceptivity (including estrous calls produced while females closely follow a target male, during post-copulatory displays, and during copulation) (Carosi & Visalberghi, 2002;Di Bitetti & Wheeler, 2017). Interestingly, the production of both visual and vocal components of these proceptive displays in black capuchin females (Sapajus nigritus) have been shown to be significantly higher during female periovulatory periods than pre-or post-periovulatory periods (Tiddi, Wheeler, & Heistermann, 2015). However, while the rate of production of the visual components of the proceptive displays have been demonstrated to be a probabilistic signal of ovulation to males (i.e.…”