Mixed messages: wild female bonobos show high variability in the timing of ovulation in relation to sexual swelling patterns

Abstract

BackgroundThe evolution of primate sexual swellings and their influence on mating strategies have captivated the interest of biologists for over a century. Across the primate order, variability in the timing of ovulation with respect to females’ sexual swelling patterns differs greatly. Since sexual swellings typically function as signals of female fecundity, the temporal relation between ovulation and sexual swellings can impact the ability of males to pinpoint ovulation and thereby affect male mating strategies. Here, we used endocrine parameters to detect ovulation and examined the temporal relation between the maximum swelling phase (MSP) and ovulation in wild female bonobos (Pan paniscus). Data were collected at the Luikotale field site, Democratic Republic of Congo, spanning 36 months. Observational data from 13 females were used to characterise female swelling cycles (N = 70). Furthermore, we measured urinary oestrone and pregnanediol using liquid chromatography–tandem mass spectrometry, and used pregnanediol to determine the timing of ovulation in 34 cycles (N = 9 females).ResultsWe found that the duration of females’ MSP was highly variable, ranging from 1 to 31 days. Timing of ovulation varied considerably in relation to the onset of the MSP, resulting in a very low day-specific probability of ovulation and fecundity across female cycles. Ovulation occurred during the MSP in only 52.9 % of the analysed swelling cycles, and females showed regular sexual swelling patterns in N = 8 swelling cycles where ovulation did not occur. These findings reveal that sexual swellings of bonobos are less reliable indicators of ovulation compared to other species of primates.ConclusionsFemale bonobos show unusual variability in the duration of the MSP and in the timing of ovulation relative to the sexual swelling signal. These data are important for understanding the evolution of sexual signals, how they influence male and female mating strategies, and how decoupling visual signals of fecundity from the periovulatory period may affect intersexual conflict. By prolonging the period during which males would need to mate guard females to ascertain paternity, the temporal variability of this signal may constrain mate-guarding efforts by male bonobos.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0691-3) contains supplementary material, which is available to authorized users.

Comparison of male conflict behavior in chimpanzees(Pan troglodytes)and bonobos(Pan paniscus), with specific regard to coalition and post‐conflict behavior

“…This difference occurs because the sexual swellings of female bonobos predict fecundity less accurately than those of female chimpanzees in two ways. Firstly, female bonobos have longer maximally tumescent swelling phases than female chimpanzees and they exhibit more variation in the date of ovulation in relation to maximum tumescence (Deschner, Heistermann, Hodges, & Boesch, ; Douglas, Hohmann, Murtagh, Thiessen‐Bock, & Deschner, ; Reichert et al, ). Secondly, during the 3–5 year inter‐birth interval, female bonobos exhibit more sexual swelling cycles that do not encompass a fertile phase than female chimpanzees do (Deschner & Boesch, ; Furuichi, ; Wrangham, ).…”

Food Sharing across Borders

“…Second, the social selection hypothesis, which postulates the occurrence of competition for being chosen as either a social partner or a mate (West-Eberhard 1983 ), could also explain tolerant sharing with unfamiliar individuals. This hypothesis finds support in the bonobos’ concealed ovulation, making mate guarding and male-male competition less effective than in other species, and giving way to female choice (Douglas et al 2016 ; Furuichi et al 2012 ; Reichert et al 2002 ). If tolerance is a trait that females select in the context of mate choice, a male displaying tolerance across community boundaries might enhance his reproductive success.…”

Inter‐group aggressive interaction patterns indicate male mate defense and female cooperation across bonobo groups at Wamba, Democratic Republic of the Congo

“…Additionally, females have priority of access to food (Furuichi, ; Parish, ; White & Wood, ). Females have prolonged periods of sexual acceptability, where their sexual swellings come into maximal tumescence not only when they are cycling but also during pregnancy and lactation (Douglas, Hohmann, Murtagh, Thiessen‐Bock, & Deschner, ; Furuichi, ; Ryu, ). This might lower the male monopolization potential of females and make males invest less in female defense, which might lead to moderate male competition (Furuichi, , ).…”