Female bonobos engaged more in genito-genital rubbing when their sexual swelling was in the maximum phase, exchanging grooming & sex according to the daily “market fluctuations” associated with swelling status

Sex and grooming as exchange commodities in female bonobos’ daily biological market. Simone Anzà, Elisa Demuru & Elisabetta Palagi. Scientific Reports volume 11, Article number: 19344. Sep 29 2021. https://www.nature.com/articles/s41598-021-98894-w

Abstract: The Biological Market Theory (BMT) posits that cooperation between non-human animals can be seen as a mutually beneficial exchange of commodities similarly to what observed in human economic markets. Positive social interactions are commodities in non-human animals, and mutual exchanges fulfilling the criteria of the BMT have been shown in several species. However, the study of biological markets suffers from methodological limitations that are mainly linked to the difficulty of clearly identifying the currencies and their exchanges in the short-term. Here, we test whether bonobo females are more attractive during their maximum swelling phase, whether they exchange grooming and Genito-Genital Rubbing (GGR) on a daily level of analysis, and whether these daily exchanges fulfil the BMT criteria. Females engaged more in GGR when their sexual swelling was in the maximum phase. Moreover, they exchanged grooming and sex according to the daily “market fluctuations” associated with swelling status. Females in the minimum phase (low-value) increased their probability to engage in GGR with females in the maximum phase (high-value) by grooming them preferentially. In line with the supply/demand law, the female grooming strategy varied depending on the daily number of swollen females present: the higher the number of swollen females, the lower the individual grooming preference. As a whole, our study confirms BMT as a valid model to explain daily commodity exchanges as a function of the temporary value of traders, and underlines the importance of a day-by-day approach to unveil the presence of a biological market when the value of traders frequently changes.

Discussion

Taken together, our results confirm the key role of sexual swelling in bonobos and provide new insights on the exchange of grooming with sex on a daily basis. More particularly, our study shows that grooming and sex represent valuable exchange commodities for bonobo females and that their exchange fluctuates depending on females’ sexual swelling status. These daily fluctuations can be explained by the supply/demand law1. In line with other studies on sexual swelling and socio-sexual behaviour in bonobos35,36, our results confirmed that females engaged significantly more in Genito-Genital Rubbing (GGR) when at least one female of the dyad was in the maximum swelling phase, compared to when both of them were in the minimum swelling phase (Prediction 1). When in the maximum swelling phase, females are more attractive for both males and females and tend to be invited more frequently to engage in sexual interactions than females in the minimum swelling phase26. This is in line with the hypothesis proposing that the peculiar features of bonobo females’ sexual swelling, and in particular its extremely long duration and presence during anovulatory periods, might have been selected to increase female-female sexual interactions35. Socio-sexuality in bonobo females help establishing and maintaining strong social bonds which, in turn, allow them to form coalitions that increase their social status and centrality30.

According to the Biological Market Theory derived from the Market Theory applied in economics, the exchange rate of commodities depends on the supply/demand law, and when a certain commodity becomes common, its perceived value decreases. Consistent with the supply/demand law, the daily grooming preference was significantly affected by the number of females showing the sexual swelling at the maximum phase during the same given day: the higher the number of swollen females, the lower the daily grooming preference (Prediction 2a, Fig. 1). Interestingly, when both the actor and the receiver were in the minimum swelling phase, and there were no females available in the maximum swelling phase, the grooming preference was very high. Via Model 1 we considered the directional grooming preference and we included the preference of both dyads AB and BA. Therefore, our results suggest that females exchanged grooming for grooming when both in the minimum swelling phase. Moreover, the significant effect of the interaction swellingact*swellingrec showed higher grooming preference when both the actor and the receiver were in the maximum swelling phase, compared to when the actor was in the minimum and the receiver was in the maximum swelling phase. These results confirm the higher attractiveness of females showing the maximum swelling phase (Prediction 1, 2b), suggest that females tend to exchange grooming for grooming when their value is “low” (MIN) and that high-value females (MAX) prefer “high-value” grooming partners as well.

Our results on the effect of the number of swollen females on grooming preference are in line with a study on male–female grooming in captive chimpanzees11 showing that females in the maximum swelling phase receive more grooming. Although our investigation focussed on female-female sexual interactions, our results are in line with those of chimpanzees given that the highest daily preference was achieved when both actor and receiver were in the maximum swelling phase. The results coming from the two Pan species are comparable considering the high attractiveness of the maximum sexual swelling in both chimpanzees and bonobos although in chimpanzees the sexual swelling is attractive for males only, while in bonobos this signal is attractive for both sexes.

In many primate groups, higher-ranking subjects typically receive more grooming than lower-ranking ones51,52,53 and most of the grooming occurs between subjects with similar rank54. Among bonobos, the distribution of grooming is related to several variables (e.g., age, rank, and sex) and there are some indications that high-ranking and older females are preferred grooming partners55. Subjects within the same group may therefore compete for grooming access to high-ranking groupmates, since those can be the best coalition partners52,54. Alternatively, a grooming distribution related to rank can be explained by females’ preference in grooming subjects of similar social class (e.g., rank and age) as an adaptive strategy derived from greater compatibility between subjects56. These mechanisms are beyond the aim of our investigation but can still drive the variation of grooming preferences and mask the effect of the daily market. For this reason, we included in our models rank and age of both actor and receiver as control predictors. However, our results on the daily grooming preference showed no effect of actor and receiver’s rank and age, suggesting that the factors shaping grooming preference among bonobo females on a daily basis may not coincide with those affecting such preference on the long term. Moreover, it has been showed that the steepness of the hierarchy varies between different bonobo groups in captivity20,25. Particularly, these studies demonstrated that grooming was preferentially directed towards dominant individuals in those groups where the hierarchy was very steep, whereas grooming was more reciprocal in those groups showing a mild hierarchy. It is worth noting that the steepness of our study groups was extremely low (Apenheul: 0.346; La Vallée: 0.305 unpublished data).

The daily occurrence of GGR was significantly affected by the number of females in the maximum swelling phase: the higher the number of swollen females, the lower the daily occurrence of GGR (Prediction 3a). Post-hoc analyses revealed no significant effect of grooming preference on the daily occurrence of GGR when the actor was in the maximum swelling condition and the receiver was in the maximum or minimum swelling condition (Fig. 3b). On the other hand, when an actor in the minimum swelling phase preferentially groomed a receiver in the maximum swelling phase, it significantly increased the probability of engaging in GGR compared to when the receiver was in the minimum swelling phase (Prediction 3b, Fig. 3a). This might indicate that: (1) when both partners are in the minimum swelling phase, none of them has the “economic power” to influence the exchange of goods and grooming is therefore not exchanged with sex (Fig. 3a; MIN-MIN), and that (2) lower-value females (MIN) need to provide more grooming to get the access to higher-value partners (Fig. 3a; MIN–MAX). However, this strategy seems to work only when is the receiver (of grooming/sexual invitations) who benefits from the mismatch, especially if we consider that an increase of grooming performed by a high-value actor does not increase the chances of engaging in sexual interactions: a high-value actor has a constant chance of engaging in sexual interactions despite receiver’s value (Fig. 3b; MAX–MIN, MAX-MAX). The results from Model 1 and Model 2 are consistently stressing that grooming can be performed to balance the mismatch in females’ value, and when the partners have equal value, grooming can be exchanged for grooming as well.

Females in the minimum swelling phase exhibit a short-term strategy of exchanging commodities shaped by the supply/demand law and receiver’s value. Given that females in the maximum swelling phase are more sexually (and therefore socially) attractive, females in the minimum swelling phase must augment the commodity they provide to increase their possibility of engaging in sexual interactions with higher-value females. Furthermore, by strategically offering more grooming, lower-value females can even outcompete higher-value ones to gather “sexual favours” from the most attractive partners.

In conclusion, our study confirms the BMT in explaining the daily exchange of commodities and its fluctuations as a function of the temporary value of traders, and underlines the importance of a day-by-day approach to unveil the presence of a biological market when the value of traders rapidly changes.