Abstract: Despite considerable cultural differences, a striking uniformity is argued to exist in human preferences for concealing sexual intercourse from the sensory perception of conspecifics. However, no systematic accounts support this claim, with only limited attempts to understand the selective pressures acting on the evolution of this preference. Here, I combine cross-cultural and cross-species comparative approaches to investigate these topics. First, an analysis of more than 4572 ethnographies from 249 cultures presents systematic evidence that the preference to conceal mating is widespread across cultures. Second, I argue that current anthropological hypotheses do not sufficiently explain why habitual concealment of mating evolved in humans but is only seldom exhibited by other social species. Third, I introduce the cooperation maintenance hypothesis, which postulates that humans, and a specific category of non-human species, conceal matings to prevent sexual arousal in witnesses (proximate explanation). This allows them to simultaneously maintain mating control over their partner(s) and cooperation with group members who are prevented from mating (ultimate explanations). I conclude by presenting a comparative framework and predictions to be tested across species and human cultures.
3. Hypotheses on the function of concealed mating in humans and their limitations
Widespread human behaviours are strong candidates for evolutionary adaptations. Their functions should therefore also be studied from an evolutionary perspective [5,19]. I thus now turn from an ethnographic survey on the prevalence of concealed mating to an evolutionarily based investigation of its function.
To date, only brief explanations have been suggested for the function of concealed mating (e.g. a few sentences or a footnote). To the best of my knowledge, the first explanation was proposed in 1930 by Malinowski, who argued that public mating ‘excites jealousy. Hence to make love or to eat in public is to invite rivals to seize that which is being enjoyed' ([6], p. 179). Half a century later, Symons repeated a similar argument: ‘Ultimately, this [concealed mating] probably is the outcome of reproductive competition. Where food is scarce, and the sight of people eating produces envy in the unfed, eating is often conducted in private. While there are many societies in which everyone has enough to eat, there are no societies in which everyone can copulate with all the partners he or she desires […] The seeking of privacy for sex probably has been uniformly adaptive and hence is virtually universal among humans' ([2], p. 67).
Building on this interaction between jealousy and reproductive competition, Friedl posited the costly consequence of reproductive competition: ‘the value of hidden sex [is] to protect [the copulating pair] and the social group from the dangers of jealousy caused by competition […] for mates, [as] a degree of social harmony is a prerequisite for an individual animal's reproductive success' ([3], p. 838). Similarly, van Schaik recently hypothesized that ‘the benefit for the man is that it prevents overt contest competition for access to potentially fertile mates, which would threaten male–male cooperation' ([11], p. 184).
These explanations share the view that avoiding overt reproductive competition is the main function of concealed mating in humans, while differing in the importance ascribed to cooperation. Malinowski and Symons neglect the importance of cooperation altogether, Friedl invokes the cost of reproductive competition on ‘social harmony', and van Schaik points out the importance of male–male cooperation. However, if these hypotheses were true, I would expect to find habitual concealment of matings in many other social species. Specifically, I would expect to find concealed matings in our phylogenetically closest living relatives, the social non-human great apes (bonobos Pan paniscus, chimpanzees Pan troglodytes and mountain gorillas Gorilla beringei beringei). In these species, within-group reproductive competition is common (electronic supplementary material, appendix S7), while social cohesion is crucial for between-group competition [20–22] and, at least among chimpanzees, male–male cooperation is vital [22]. Nevertheless, dominant individuals from these species seldom conceal matings from the view of conspecifics (electronic supplementary material, appendix S7; see §4d(iv) and §5 for explanations for occasional concealment in these species).
In conclusion, although the selective pressures proposed by current explanations may have played a role in the evolution of concealed mating, in my opinion, these explanations do not sufficiently explain why habitual concealment evolved in humans but is rarely exhibited in other social great apes. I propose that explaining the currently known taxonomic distribution of concealed mating should be the first touchstone for any hypothesis aiming to explain the function of concealed mating in humans.
4. The cooperation maintenance hypothesis
In this section, I discuss the cooperation maintenance hypothesis (hereafter ‘CMH’). I first review the phenomenon of concealed mating in non-human species, while emphasizing the Arabian babbler (Turdoides squamiceps), for which this hypothesis was originally proposed [23]. Second, I develop a cross-species and cross-cultural account of the hypothesis. Third, I apply the CMH to explain the human case. Fourth, I present predictions to test the CMH across species and human cultures.
(a) Non-human species
In a wide range of species, subordinate animals conceal matings to avoid interference by more dominant group members. Dominant individuals, by contrast, often mate in full view of group members and seldom actively conceal matings (see electronic supplementary material, appendix S7 for review of 34 species and §4d(iv) and §5 for potential explanations). To my knowledge, habitual concealment of matings by individuals that are not subject to physical interruption by conspecifics has so far been documented in two species only: humans and Arabian babblers.
Arabian babblers are cooperative breeding birds living in the Middle East [24]. They live in stable, territorial groups (2–22 individuals) that include all combinations of age, sex and kin relations [24]. During days in which the alpha female ovulates, she is mate-guarded by the alpha male, who may use dominance displays when other males interact with her [25]. Consequently, the dominant pair produces 95% of the offspring [26]. Nonetheless, all group members participate in rearing offspring (e.g. transferring them between shelters [27]) and other cooperative interactions [28]. Helpers have therefore a significant effect on offspring survival [29].
Arabian babblers use discreet communication to initiate copulation [25]. Then, pairs sneak away and only mate in locations and/or times in which they are hidden from view of other group members [23]. Subordinate Arabian babblers are likely to conceal their matings since they risk attack if discovered by more dominant group members [23,25]. A subordinate bird, however, would not attack the dominant pair if it happened to interrupt the privacy of mating [23,25]. After presenting evidence against common explanations for inconspicuous matings in non-human species (see §5), Ben Mocha et al. [23] proposed that dominant Arabian babblers conceal visual stimuli of mating to (i) avoid triggering extra-pair matings by helpers and (ii) maintain alloparental care (by avoiding conflicts that would increase the probability of helpers challenging the alpha position or dispersing).
(b) The cooperation maintenance hypothesis: cross-species and cross-cultural account
The CMH is based on the following argument:
If:
(i)
Sensory stimuli of mating between conspecifics evokes sexual arousal and trigger mating behaviour in witnesses (hereafter, the sexual arousal premise).
(ii)
X (a male and/or a female) tries to control mating access to his/her partner(s) (hereafter, the mating control premise).
(iii)
X depends on cooperation with group members that he/she prevents from mating with his/her partner(s) (hereafter, the cooperation dependency premise).
Then:
Public mating between X and his/her partner will evoke sexual arousal in group members (males and/or females). This, in turn, will increase the likelihood that aroused witnesses will attempt to initiate mating with X's partner when possible (the sexual arousal premise). These attempts will violate X's efforts to control mating access to his/her partner (the mating control premise) and will trigger social conflicts that will harm the cooperation between X and his/her group members (the cooperation dependency premise; figure 1).
[Figure 1. The predicted consequences of concealed and public mating in social systems where an individual tries to control mating access to all or specific partner(s), while also dependent on cooperation with group members that are prevented from mating with his/her partner(s). (Online version in colour.)]
By contrast, sensory concealment of X's mating with his/her partner will not evoke sexual arousal in group members. Hence, the act of mating will not induce extra-pair mating with X's partner and will not affect X's cooperation with other group members (figure 1). I therefore suggest that concealed mating by individuals whose mating is not subject to physical interruption by conspecifics is a relatively non-costly strategy for avoiding unnecessary sexual arousal in group members (proximate explanation). At the ultimate level, concealed mating allows an individual to maintain two needs that would otherwise conflict: mating control over his/her partner(s) and cooperation with those group members that are prevented from mating with these partner(s).
Thus, the CMH elaborates factors that were previously proposed to select for concealed mating—jealousy [2,6], reproductive competition [2,3,11] and social harmony/male–male cooperation [3,11]—and combines them as necessary premises of a coherent argument. According to the CMH, explanations that rely solely on avoiding reproductive competition [2,6] are not sufficient, since the question of concealed mating is only applied to individuals who do not expect interference from conspecifics (e.g. dominant individuals). In addition, in social systems without cooperation, dominant animals settle conflicts with aggression and often mate in public (e.g. Rocky Mountain bighorn sheep Ovis Canadensis [30]). But where competitors also cooperate, aggression may eliminate future cooperation (for ethnographic examples in Yanomamö see [31]). The CMH differs from previous explanations by requiring both a specific form of reproductive competition (i.e. attempting to prevent group members from mating with one's partner) and reliance on cooperation between group members. It thereby highlights the need to manoeuvre between these conflicting motives as the crucial selective pressure.
The CMH further stands up to evolutionary critiques that previous explanations failed to address. Namely, it can explain why dominant individuals of non-human great apes seldom conceal mating: because they rarely monopolize a specific partner (bonobos and chimpanzees use other forms of reproductive competition, e.g. sperm competition [32]; electronic supplementary material, appendix S7]) or they do not depend on cooperation with subordinate group members (mountain gorillas; electronic supplementary material, appendix S7)—at least not to the same extent as humans and Arabian babblers (but see §4d(iv)).
(c) Explaining the human case
In the following, I discuss the evidence that supports the three premises of the CMH in humans.
(i) Sensory stimuli of mating between conspecifics evoke sexual arousal and trigger mating behaviour in witnesses
Visual [33] and auditory [34] stimuli of mating activate the reward system in the human brain and trigger mating behaviour in males and females via mirror neurons. For ethnographic examples, see the Goajiro [35] and Lesu [16].
Knowing that a desired group member has a legitimate mating tie with another person may also trigger jealousy (see the Muria for ethnographic examples [18]). Yet, the sensory stimulus of mating is another powerful trigger of sexual arousal that can be prevented by sensory concealment. The benefits of sensory concealment therefore do not rely on individuals being ignorant of the existence of mating ties between group members.
(ii) X (a male and/or a female) tries to control mating access to his/her partner(s)
Various scholars have claimed that in virtually all cultures, husbands and/or wives try to control mating access to their spouse(s)—at least to a certain degree [1,2,9,36]. Three clarifications should be made regarding this claim. First, mating control should not be confused with monogamy. For instance, a man/woman may marry several wives/husbands and forbid them to have extramarital sex. Second, it has been argued that even in cultures where some extramarital sex is allowed (e.g. in cultures with ‘shared paternity'), husbands and/or wives are still entitled to restrict the trysts of their spouse(s) to specific individuals and/or limit extramarital sex to the greatest possible extent [9]. Third, this premise requires an attempt, not a success, to control mating access to X's spouse(s). As adultery is evident across human societies [10], this emphasizes the importance of behavioural strategies to reduce its occurrence.
Although it has been claimed repeatedly that restrictive sexual norms are virtually universal, there is a dearth of supporting evidence (but see [1,9]). Hence, I analysed whether social norms in this study's dataset entitle husbands and/or wives to at least some control over mating access to their spouse(s), or, in contrast, if both spouses are allowed to have unrestricted extramarital sex (see electronic supplementary material, appendix S1 for methodology). I found social norms that entitle mating control over spouse(s) in 100% of cultures for which data were available (survey dataset: n = 210; SCCS/EA dataset: n = 145; see electronic supplementary material, appendix S8 for full account). Cultures had diverse norms of sexual control; for instance, norms that forbid both spouses to have extramarital sex (e.g. orthodox Jews [37]); cultures where wives are required to stay faithful to their husbands, but husbands are allowed to have extramarital sex (e.g. Malekula [38]); and cultures where husbands and/or wives are allowed to have extramarital sex, but only with specific partners (e.g. Huaorani [39]). I found no culture in which social norms entitle both husbands and wives unrestricted freedom to engage in extramarital sex. These norms suggest that in virtually all human societies, group members are prevented (sometimes or always) from mating with spouses of others.
(iii) X depends on cooperation with group members that he/she prevents from mating with his/her partner(s)
Humans depend on cooperation with group members in various aspects, such as hunting and between-group competition (e.g. [31]). Furthermore, an individual's fitness critically depends on systematic alloparental care from kin and non-kin [40]. For example, the survival of parents and offspring in hunter–gatherers Hiwi (Venezuela) and Ache (Paraguay) depends on food obtained by young, unrelated males [41]; infants of the Aka people in central Africa are carried by kin and non-kin helpers for roughly 30% of the time [42]. Humans are thus considered a communal, and even cooperatively breeding, species [40].
(iv) Summary
In conclusion, visual and audile stimuli of human mating trigger sexual arousal and sexual behaviour in both male and female observers [33,34]; across cultures, husbands and/or wives attempt to control mating access to their spouse(s) (electronic supplementary material, Appendix S8, [9]); humans live in social systems where fitness crucially depends on cooperation between group members [40,41]. I therefore suggest that the habitual concealment of legitimate mating in humans is a relatively non-costly behavioural strategy to prevent unnecessary sexual arousal in group members (proximate explanation). This simultaneously maintains control over mating access to their spouse(s) as well as cooperation with group members that are prevented from mating with their spouse(s) (ultimate explanations).
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