Physical, behavioral, and hormonal changes in the resumption of sexual receptivity during postpartum infertility in female bonobos at Wamba

Abstract

The operational sex ratio (OSR) is used as a predictor for the intensity of mating competition. While many factors affect the OSR, there tends to be a high male bias in primate species with long interbirth intervals and non-seasonal breeding, such as hominid apes. However, the OSR of bonobos (Pan paniscus) is lower than that of chimpanzees (Pan troglodytes), which is thought to reduce competitive and aggressive male behaviors. The low OSR of bonobos is considered to result from the early resumption of female sexual receptivity during postpartum infertility and the receptivity that they continue to show until the late stage of pregnancy. In this study, we aimed to examine the early resumption of sexual receptivity by providing quantitative data on the resumption of maximal swelling (MS) in sexual skin and copulation, and changes in urinary estrone conjugate (E₁C) concentrations during postpartum infertility in wild bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo. An analysis of 9 years of data revealed that females showed the first MS at 225.4 ± 132.7 days after parturition and performed the first copulation at 186.8 ± 137.5 days after parturition, both of which were in the early stage of postpartum infertility. The proportion of days with MS and the frequency of copulation steadily increased subsequently; however, the rate of increase gradually slowed approximately 42-48 months after parturition. There was a significant correlation between the proportion of days with MS and the frequency of copulation in each period for each female. We confirmed that E1C concentrations were significantly higher during the MS phase than during the non-MS phase. Data collected over 15 months on the E₁C concentration during MS showed that it increased linearly from the early stage of lactation to the next conception. These results suggest that, although female bonobos do not usually conceive until 49.7 months after parturition, they resume MS and receptivity at a low level of E₁C concentration during an early stage of postpartum infertility. This study of female bonobo receptivity and sex hormone changes during the postpartum non-fertile period provides important insights for examining the evolution of low OSR, which has been considered to contribute to peaceful social relationships among bonobos.

Keywords: Bonobo; Copulation; E1C concentration; Operational sex ratio; Pan paniscus; Postpartum infertility; Sexual swelling.

Fig. 1

Changes in the proportion of observation days with maximal swelling (MS) with increase in time after parturition (model 1). Each dot represents one female in each 6-month period (N = 113 for 21 interbirth intervals of nine females). The x-axis shows the duration in months from parturition to the midpoint of each 6-month period. The y-axis shows the proportion of MS in each 6-month period. Some females have two dots in the same period because they had two parturition events during the study period. The blue line shows the fit of the model including the linear and squared terms of the number of months after parturition, and the grey shading shows the 95% confidence area of the fitted line

Fig. 2

Changes in the frequency of copulation with increase in time after parturition (model 2). Each dot represents one female in each 6-month period (N = 113 for 21 interbirth intervals of nine females). The x-axis shows the duration in months from parturition to the midpoint of each 6-month period. The y-axis shows the number of copulations observed per day of observation in each 6-month period. Some females have two dots in the same period because they had two parturition events during the study period. The blue line shows the fit of the model including the linear and squared terms of the number of months after parturition, and the grey shading shows the 95% confidence area of the fitted line

Fig. 3

E₁C concentrations in each swelling status (model 3). The unit of analysis is each urine sample of each female. The middle lines represent the median values of all urine samples in each swelling status. Boxes represent quartile ranges; whiskers represent maximum and minimum values excluding outliers shown by dots

Fig. 4

Changes in E₁C concentrations with increase in time after parturition (model 4). The x-axis shows the duration in months from parturition. The y-axis shows the median E₁C value during MS for a given female in a given 1-month period (N = 47 for eight interbirth intervals of eight females). We log-transformed the value to fit the normal distribution. The blue line shows the fit of the model including the linear term of the number of months after parturition, and the grey shading shows the 95% confidence area of the fitted line