RESEARCH ARTICLE Open Access Blackmailing: the keystone in the human mating system Milind G Watve1,2*, Anuja Damle2, Bratati Ganguly3, Anagha Kale2 and Neelesh Dahanukar1 Abstract Background: The human mating system is characterized by bi-parental care and faithful monogamy is highly valued in most cultures. Marriage has evolved as a social institution and punishment for extra pair mating (EPM) or adultery is common. However, similar to other species with bi-parental care, both males and females frequently indulge in EPM in secrecy since it confers certain gender specific genetic benefits. Stability of faithful monogamy is therefore a conundrum. We model human mating system using game theory framework to study the effects of factors that can stabilize or destabilize faithful committed monogamy. Results: Although mate guarding can partly protect the genetic interests, we show that it does not ensure monogamy. Social policing enabled by gossiping is another line of defense against adultery unique to humans. However, social policing has a small but positive cost to an individual and therefore is prone to free riding. We suggest that since exposure of adultery can invite severe punishment, the policing individuals can blackmail opportunistically whenever the circumstances permit. If the maximum probabilistic benefit of blackmailing is greater than the cost of policing, policing becomes a non-altruistic act and stabilizes in the society. We show that this dynamics leads to the coexistence of different strategies in oscillations, with obligate monogamy maintained at a high level. Deletion of blackmailing benefit from the model leads to the complete disappearance of obligate monogamy. Conclusions: Obligate monogamy can be maintained in the population in spite of the advantages of EPM. Blackmailing, which makes policing a non-altruistic act, is crucial for the maintenance of faithful monogamy. Although biparental care, EPM, mate guarding and punishment are shared by many species, gossiping and blackmailing make the human mating system unique. Background Cooperation is commonly accompanied by cheating or defection in a number of naturally occurring social sys- tems [1-4]. In Prisoner���s Dilemma (PD), the popular model of cooperative behaviour, cooperation is not stable and defection is the only stable strategy for any player [5]. However, in iterated PD games strategies involving reciprocity or reputation can help stabilize cooperation [5,6]. If the same individuals play the game again, defec- tion can be retaliated [5]. Furthermore, cooperators can build a reputation and derive long term gains from it [6]. Cooperation can also evolve if co-operators punish those who defect [7-9]. However, a potential problem in pun- ishment is that there is a cost in executing punishment, which makes punishment an altruistic act. Since the ben- efits derived by punishing cheaters are shared, there arises a possibility of second order free riders that coop- erate but do not contribute to punishment. The second order free riders can destabilize punishment and coop- eration in turn. A number of conditional solutions to this problem have been suggested [8-10]. One of the basic assumptions behind all suggested solutions to the problem of stability of cooperation is that the strategies of players and the resulting payoffs are open at the end of every interaction. Retaliation, punish- ment or reputation is possible only if players have access to the history of other players and would fail to work for games in which the strategies and payoffs remain hidden. In a number of real life games it is possible that the players have a choice of secrecy or deception. Evolution is likely to take a different path when the strategies as * Correspondence: milind@iiserpune.ac.in 1Indian Institute of Science Education and Research, Sai Trinity Building, Pashan, Pune 411021, India Full list of author information is available at the end of the article Watve et al. BMC Evolutionary Biology 2011, 11:345 http://www.biomedcentral.com/1471-2148/11/345 �� 2011 Watve et al licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

well as payoffs remain hidden from the players most of the time. The human mating system is an ideal and obvious example of hidden strategy games. Since paternity is uncertain the actual reproductive success of a male remains hidden. For females although some of the compo- nents of benefits, for example resource partitioning and the number of offspring borne by them is obvious, the genetic contributor to the offspring and therefore the ben- efit of ���good genes��� remains hidden. It is possible to apply game theoretic models human mating system considering faithful long term bi-parental care as cooperation and extra-pair mating (EPM) or cuckoldry as defection [11]. In a number of species where biparental care is necessary, EPM or cuckoldry is known to be common [12-21]. Human marriage system is more complex than other spe- cies with bi-parental care in that marriage is not only a game of cooperative partnership but it is a social institu- tion. Although societal rules differ regarding the allowed number of spouses at a time [22], long term investment and faithful commitment by both genders in childcare is central to the system. Further, faithful monogamy is highly valued in most cultures. There are likely to be multiple reasons for the evolution of a committed marriage system, the main reason being the prolonged dependence of the human child. Biparental care and division of labor is necessitated by the extreme human newborn altriciality, demand of multiple simultaneous dependents and longer period for maturity [23,24]. As a general rule, sexual dimorphism in size is shaped by the mating system, with most promiscuous species showing maximum dimorphism and those with monogamy and biparental care showing lit- tle dimorphism. In human evolution, size dimorphism is low through most of the Homo and pre-homo lineage indicating that mating system could be stable over time. It is reasonable to assume therefore that monogamy is evolu- tionarily ancient in hominids [25]. Although biparental care necessitates cooperation, it may not be sufficient to maintain faithful monogamy as occult polygamy can con- fer added genetic benefits to both the genders. Thus, simi- lar to other species with biparental care, EPM or cuckoldry is known to occur at varying frequencies in the human society as well [12,18,20,21,26,27]. In cuckoldry, the polygamous individuals get an additional genetic advantage, but their mates have to bear a loss. Males can increase their number of offspring by indulging in EPM. The benefits are not in terms of number of offspring for females. The advantage of EPM for females can be in terms of additional resource acquisition, sperm competi- tion or getting dual benefit of good parenting from one male and good genes from another [20,28-31]. Males suf- fer a direct genetic loss by their partner���s EPM since their paternity is threatened [26]. The loss to females is less obvious since their maternity is never threatened. However, they may suffer in other ways like loss of the man���s time, attention, energy, parenting investment, and commitment [19,21]. The human mating system as a hidden strategy game differs from the games of incomplete information [32] in that, not only the strategy and payoff of the other player is hidden but the payoff of the focal player also remains hid- den. Since there are few opportunities to learn from pay- offs, learning is less likely to shape the behaviour but natural selection would certainly continue to act at the genetic level. Therefore human sexual behaviour is more likely to be dominated by instincts rather than learning. Two types of measures against cuckoldry are seen in the human society, namely mate guarding [19,20], a trait shared by many species [33-36], and societal punishment if cuckoldry gets exposed [11] which appears to be uniquely human. Although the probability of getting exposed is small its consequences are known to be severe in most human societies and exposed adulterous individuals gener- ally receive punishment in some or the other form. Altruis- tic punishment or strong reciprocity has been used in the models of evolution of cooperation [7,8,37]. However, altruistic punishment suffers from the problem of second order free riders [37,38]. In the human mating system there can be a non-altruistic punishment in the form of social sanctions. If an adulterous individual is deserted by its partner who makes the reason public, the probability of pairing again could be very small for the deserted indivi- dual, a form of ostracism or community boycott [39,40]. While for the deserting partner, if the probability and the net benefit of pairing again is higher than the net benefit from continuing partnership with a known defector, deserting would be a non-altruistic way of punishing. Avoiding pairing with a known defector is also a non- altruistic act. Therefore, punishment for cuckoldry by the partner as well as by the society need not have an altruistic element in it at least in its minimal form. More complex punishment systems appear to have evolved in complex societies but the basic form of minimal punishment in terms of social sanctions can be considered non-altruistic. However, since individuals have the choice of secrecy, if the probability of getting exposed remains small, punish- ment may fail to curb EPM. The stability of monogamy would depend upon mechanisms to increase the probabil- ity of exposure. In humans, due to evolution of language, gossip is possible through which one can gain information about the behaviour of a sexual partner in one���s absence. In fact the need to gossip has been argued to be one of the major selective forces for the evolution of language [41]. This is an indirectly reciprocating, apparently altruistic social act that forms a component of ���social policing���. Social policing consists of making observations about others��� EPM and its indicators on the one hand and gos- siping about it on the other. The cost involved in social Watve et al. BMC Evolutionary Biology 2011, 11:345 http://www.biomedcentral.com/1471-2148/11/345 Page 2 of 11