Sexual Paradox: Complementarity, Reproductive Conflict and Human Emergence Sexual Paradox: Complementarity, Reproductive Conflict and Human Emergence
"All's fair in love and war" leads us to a point of no return. To all intents and purposes, love is the uniting force of empathy and requital, and war is the ultimate Armageddon, conflict run amok on a collective scale. How can the two ends of the spectrum be so indistinguishably entwined? What does this spell out about our striving for unity in the face of disunion? What hope do we have of reaching a resolution, if love and war are so equatable - indeed equitable - as if dark and light were simply faces of one another? And what does it mean to say that ALL is fair, as if every position we could take, from integrity to deceit, from faithfulness to betrayal, are all legitimate players of a summer game? And how do we successfully negotiate these paradoxically entwined paths, one of which leads to a wasteland of attrition, wounding and death and the other to paradoxical reunion, completion, abundance and life? This is the answer to the Prisoners' Dilemma in sexual paradox.
Of course, life is a game we can never escape except in death. The evolutionary struggle is no better, doomed to a purgatory of survival amid conflict and cooperation, so long as our genes mutate and survive. The only culmination of this game is extinction. The outright wins all animals have, in the predatory process of feeding, are merely another step on the road of survival, staving of the hour of final reckoning.
The Prisoners' Dilemma as a classical game matrix. Payoffs for each player are such that each is 'tempted' into defection, resulting in mutual nemesis. Attempts to resolve the devastating simplicity of the matrix may involve conditional strategies (e.g. I'll do what you do) or mixed strategies playing both strategies with probabilities. Real tournaments also involve repeated and sequential exchanges, which encourage cooperation, at least until the last round or two.
The Prisoners' Dilemma
The Prisoners' Dilemma is a universal paradox in game theory in which mutual defection leads to the 'double jeopardy' of collective downfall. In the classic case, two criminals are to be tried for a joint offence. If one betrays the other and becomes an informant, they will get protection, but the other will go down as the ringleader with no parole. If they both stay silent, they will only get done for a minor offence, but if both defect and spill the beans they will get a jail term for conspiracy. If the game is played only once, any rational player will defect. If they cooperate in silence they will at best get a minor felony and worst no parole, but if they defect, they might get sprung with a middle term, or they might get off with a non-custodial sentence. However an astute player facing repeat encounters will be much more canny and cooperate, at least until the last round's high noon.
Joseph Heller's "Catch 22" (R306), describes a classic form of the Prisoners' Dilemma as a logically paradoxical double bind. With a growing hatred of flying, Yossarian pleads to be grounded on the basis of insanity. His appeal is however useless because, according to army regulation Catch-22, insane men who ask to be grounded prove themselves sane through a concern for personal safety. The only truly crazy people are those who readily agree to fly more missions. The only way to be grounded is to ask for it, yet this act demonstrates sanity and thus demands further flying. Crazy or not, Yossarian is stuck.
The Prisoners' Dilemma is a root paradox permeating all areas of knowledge, from the stability of rational assumptions of best interest in economics (R102) to the fractal complexity of climax forests (p 506). It's status has been acknowledged by economists and utopian thinkers, from Hobbes to Rousseau. All its diverse forms involve the splitting of a process, under increasing polarization into competing domains leading to nemesis - any situation in which the participating entities are 'tempted' into a course of action which would bring disaster if everyone did the same thing. The game applies in a chilling manner to the risks of nuclear war and the knife-edge advantage of first strike.
Ironically one of the first people to introduce the concept of cooperation into a view of nature as a pitiless "war of each against all" as Thomas Huxley described it in Hobbes' words, was the Russian anarchist Prince Petr Kropotkin (Ridley R578), who had himself escaped prison in a daring ingenious feat of cooperative insurrection. In 'Mutual Aid' (R395) he rejected the notion that selfishness is an animal legacy and morality a civilized one, claiming that supportive species were fitter than those endlessly at war, challenging a long tradition, going back through Malthus and Machiavelli to Augustine, shared today in the stress on competition as a motivating force for the free market. We can see in Kropotkin's twist of fate just how conducive to 'inscrutable cooperation' in a Machiavellian context, the Prisoners' Dilemma can be. Kropotkin's work emphasizing the role of cooperation and his intuitive opposition to an exclusive focus on competition has recently received recognition from authors as diverse as Ridley (R577) and de Waal (R162).
The cusp, the first of Rene Thom's classical catastrophes (R686) enters criticality, causing the process to bifurcate between competing regimes. As x passes through 0 the surface folds, causing cooperation to move into competition, and behavior to flip between fight and flight. Prisoners' dilemma games attempt to resolve the disparity between these two conditions and their varying payoffs.
The Prisoners' Dilemma became transformed into the battleground of the genetic arms race by the work of evolutionary biologists George Williams and William Hamilton in the 1960s epitomized by Richard Dawkins (R151) infectious phrase "the selfish gene". This shifted the pendulum from collective concepts, of 'survival of the species' and 'group selection' to a detailed analysis of how genes act as agents of their own selection in a way which leaves the organism little more than a doomed collection of apparently selfish genes, barely held in check in a common, yet shifting genome. While group selection and the capacity for social selection has not been entirely extinguished, George Williams in 1966 demonstrated that it is unstable to individual defection. The primacy of genetic selection shone a new spotlight on the exact processes providing stable strategies in evolution, which are robust to defection.
The Red Queen hypothesis of sexuality (p 26) with its paradoxes between parasite and host and between female and male genetically and more particularly sexual evolution, both of which we shall examine next, are outstanding examples of the Prisoners' Dilemma. In the sexual context the Prisoners' Dilemma genetic race between female and male is also bifurcated between the differing strategies of female out-front long-term investment and the male strategies of sneaky short term fertilization and direct male-male reproductive conflict. Thus not only do we have male and female locked in a genetic race from which neither can escape, but the male strategy is prone to natural flight and fight of its own accord. This male tendency to conflict is liable to a break down of the game into a male dominance over the female, profoundly exaggerating the tendency to violence and war. Thus while the male and female are both strategic players of the game, they also represent relative extremes of the energy landscape in terms of cooperation or conflict. The emergence of patriarchal dominance in human society has been explained as a response to ecological stress (Sanday R609 181) in terms entirely consistent with a symmetry-breaking of the Prisoners' Dilemma between male and female into a protracted impasse involving crisis and instability.
The arms races that result from the Red Queen process extend via the Prisoners' Dilemma to all forms of competitive arms race, such as the mutually assured destruction from nuclear holocaust we have all continued to face since the beginning of the Cold War despite symbolic efforts at nuclear arms reduction, the knife-edge cooperator-defector zero-infinity dilemmas of launching a first strike and all runaway militarization races between competing powers, who could also cooperate to their mutual but less successfully exploitative benefit. It also applies to mediation between intergroup competition, protection from aggression and the consequent need for cooperation within groups in evolving the kinds of systems we come to associate with morality, ethics and the rule of law. Richard Alexander (R6) in "The Biology of Moral Systems" has given an in-depth analysis of the relationship between these two phenomena which has been widely applied by many researchers (p 44). Key here is the interaction between inevitable competition between groups which are large in the case of humanity and the complementary ensuing need to evoke systems of social selection which ensure the group is internally cooperative enough to remain competitive or even dominant. The theory thus explains the emergence of moral systems and ethics based on principles of natural selection, rather than cultural constructs alone. The breakdown of such moral conventions often involves the breaking of a common pact for individual gain, as when a ring of hunters joining to encircle a deer is broken by one person or another diving off after a rabbit he is sure to catch, as noted originally by Rousseau. A similar analysis by Turchin (R706) examines cycles of cooperative foundation, empire, growth of inequality, disaffection on the turbulent perimeter, and rebellion.
The Prisoners' Dilemma also comes in more complex ecosystemic forms than the one-on-one arms races of host-parasite and sexual relations . The complexity of a climax forest is the result of a prisoners dilemma relationship between many plant species competing for light. It also permeates animal species in the natural competition between the members of a population for reproductive, and food resources and for personal power and fortune. Nowak and Sigmund (R510) point out that evolutionary game theory places the usually presumed constant fitness landscape of natural selection in a feedback process, in which payoffs can be reversed by population changes, leading to rare strategies being reinforced (p 60), amid stable coexistence or unstable oscillation, or punctuated equilibrium.
A graphic illustration of the diversity of life as a Prisoners' Dilemma game caught mid-way between cooperation and defection is given by the diversification into plants and animals, (p 327). Plants are broadly cooperative although there is always competition for limiting resources since they fix their energy from sunlight rather than depending on consuming one another. Animals defect by directly consuming plants, subsequently bifurcating into second order defections in the form of predatory carnivores who also eat other animals. The earliest life forms were either phototrophs, or converted free mineral energy such as that in hydrothermal vents, so the evolution of life into diversity is a movement from initial cooperative exploitation of an external energy source, subsequently filling sufficient defection niches to provide ever-increasing diversity to climax and the pyramidal populations of food webs.
The evolutionary tree of life is our richest example of the Prisoners' Dilemma. The survival of every gene of every species is a Prisoners' Dilemma. Each gene, organism and species lives as long as its Prisoners' Dilemma of coexistence as parasite and host, predator and prey, symbiotic, saprophytic and reciprocal interactions with others of its kind. As long as we survive, we remain locked in the Prisoners' Dilemma mediation of cooperative and competitive forces that we call life. Death is a loss. The only hope is to remain in the game. This however condemns each species to evolutionary adaption through mutation. This brings in the issue of genetic algorithms and the entire concept of gene as a fundamental response to the Prisoners' Dilemma in molecular terms.
A paradigm-defining example of Prisoners' Dilemma is the 'tragedy of the commons', which Gareth Hardin (R289) used as the title of his renowned paper on the exploitation of the commons in economics (p 439). In this form of the paradox, it always pays off exploiters of the commons better to claim the competitive certainty of exploitation than the 'altruists' who cooperate to preserve the common wealth. The end result is multiple jeopardy, the commons is destroyed and every one loses out. Various forms of the tragedy of the commons underlie all of the major forms of human exploitation on the planet, from depletion of non-renewable resources to causing the mass extinction of biodiversity.
Puccini's opera Tosca well illustrates how deeply related the Prisoners' Dilemma is to sex and sexual betrayal. Tosca's lover Cavaradossi has been condemned to death by the police chief Scarpia. He offers her to tell the firing squad to use blanks if she will sleep with him. She resolves to pretend to agree to lie with him only to stab him to death as soon he has given the order. He gives a coded order to use live bullets and she stabs him, instead of submitting to his advances, only to find he has also betrayed her and executed her lover regardless. She commits suicide in despair. Double betrayal. Triple jeopardy.
The sexual relationship is from beginning to end a permanent state of Prisoners' Dilemma paradox. The two sexes are reproductively entwined, so neither can escape the other. Even parthenogenesis is only a temporary fix, until evolving circumstances, such as disease, require sexual adaption for survival. For this reason sex has remained an essential feature of higher organisms. Although the interests of the female and male coincide in reproductive fertilization, their overall reproductive strategies and genetic 'drives' are competing in significant ways, both reproductively and genetically.
In describing the dilemma of female chimps mating promiscuously with every male to avert the threat of infanticide from the males, Sarah Hrdy (R331) notes the cutting truth of William Rice's term "sexually antagonistic coevolution" (R575), emphasizing the Prisoners' Dilemma of the interaction for each sex. Increasing female choosiness in relation to the lengthening peacocks tail is an example of sexually-antagonistic coevolution, as is the race between an increasingly turgid penis and an increasingly discriminating clitoris.
Darwin noted somewhat chauvanistically: "man has ultimately become superior to woman. It is indeed fortunate that the law of equal transmission of characters to both sexes prevails with mammals. Otherwise it is probable that man would have become as superior in mental endowment to woman as the peacock is in ornamental plumage to the peahen". The fallacy of this position is itself an irony - the attribution of reproductive choice principally to females and runaway sexual selection principally to males . The realities of human sexual evolution, while they do support sperm competition and moderate polygyny speak strongly of a more complex pattern of mutual mate selection, something Darwin also recognized was possible as Geoffrey Miller has noted. It is this very complexity that we shall claim is at the centre of our cultural emergence.
William Rice's cogent commentary comes from his experiments into the mating habits of flies, where male semen reduces the subsequent fertility of the female at the expense of rearing the current male's progeny, either by plugging her, inserting digestive enzymes, or affecting her hormonally. For this reason a female house fly mates only once, because her partner's poisons are so potent she can never mate again (Jones R349). In other species of fly, where multiple mating occurs, an arms race sets in between male toxins and female resistance. Consequently these genes are the most rapidly evolving in insects. This process is accentuated when mating is frequent but diminishes when mating occurs only rarely or once in a lifetime. During fruit-fly sex, the proteins in the semen enter the bloodstream of the female and migrate to, among other places, her brain. There they have the effect of reducing the female's sexual appetite and increasing her ovulation rate. The male's seminal fluid redirects her behaviour to that end. After breeding generations of increasingly 'super-macho' male flies while allowing the females' resistance to diminish, Rice found the semen had become toxic to the point of being lethal (Friedman R227 235, Ridley R579). Hrdy (R330 41) comments that this demonstrates the way in which not only female reproductive choice but its curtailment can have profound consequences.
A fundamental characteristic of modern mammals - the birth of live young - is another extreme example of this phenomenon. The placenta is controlled by rapidly evolving paternal genes. As noted a double Y induces a placental pregnancy called a hydatidiform mole. David Haig (Ridley R579) considers the placenta to be a parasitic takeover of the mother's body by paternal genes in the fetus. The placenta tries, against maternal resistance, to control her blood-sugar levels and blood pressure to the benefit of the fetus. By contrast X-inactivation in female embryos is skewed from a random process in cells inside the embryo towards inactivating the paternally-imprinted X in the placenta (p 346). Boys also impose a greater strain on the mother, causing her to have a longer lapse until her next child, possibly increasing the chances of abnormalities in subsequent pregnancies and reducing the mothers life expectancy by about 6 months. By contrast a girl child slightly increases it. The male determining gene SRY and the female pathway driven by DAX are similarly in a state of sex-determining conflict. One SRY defeats DAX giving our usual male profile but an accidental two DAX in the genome overwhelm SRY resulting in a female (p 359). Intriguingly, endogenous retroviruses or ERVs, transmitted down the germ line of every mammal, may have also played a starring role in the evolution of mammalian life and its crowning achievement-live birth. ERVs which bloom on the placental tissue, appear to be critical to the emergence of the placental membrane and the mechanisms that protect the fetus from pathogens and the mother's immune system. Without ERVs, humans might still be laying eggs (p 333).
Ridley (R579) notes that communication itself becomes an informational pawn in the game: "Rice and Holland come to the disturbing conclusion that the more social and communicative a species is, the more likely it is to suffer from sexually antagonistic genes, because communication between the sexes provides the medium in which sexually antagonistic genes thrive. The most social and communicative species on the planet is humankind. Suddenly it begins to make sense why relations between the human sexes are such a mine field, and why men have such vastly different interpretations of what constitutes sexual harassment from women. Rice now believes that sexual antagonism is at work in an sorts of environments. It leaves its signature as rapidly evolving genes." Consistent with this, Dawkins has pointed out that 'information' serves the 'giver' only if it includes a component of self-serving deceit. This is not however true of genuine indicators of fitness, such as the peacock's tail, which have to be costly to be effective in the sexual race.
We may have genetic conflict to thank for the fact that we have feelings toward other people at all. One might at first think that evolution would endow a species in which the genetic interests of two mates were identical, with a blissful perfection of sexual, romantic, and companionate love, but, Donald Symons argues the relation between the mates would then evolve to be like the relation among the cells of a single body, whose genetic interests are also identical. There would be no falling in love, because there would be no alternative mates to choose among, and falling in love would be a huge waste. You would literally love your mate as yourself, but - you don't really love yourself, you are yourself. The same is true for our emotions toward family and friends: the richness and intensity of the feelings in our minds are proof of the preciousness and fragility of those bonds in real life. In short, without the possibility of suffering, what we would have is not harmonious bliss, but little or no emotional consciousness (Pinker R544 268).
This kind of conflict between complexes of genes does not just apply to sex but to all forms of deceit and detection of cheating the Prisoners' Dilemma game implies. A gene that increases the telling of lies might thrive by making its possessors successful con-artists. But then any set of genes that improves the detecting of lies would thrive to the extent that it enabled its possessors to avoid being taken in. The two would evolve antagonistically, each gene encouraging the other, even though it would be quite possible for the same person to possess both. Rice and Holland call this 'interlocus contest evolution' (R576). If the conflicting genes are on different chromosomes or not closely linked they can both evolve. The signature of such genes is rapid evolution and in comparing human and mouse genomes, such genes are notably found in immunity and sex determination.
Ridley notes: "Exactly such a competitive process probably did indeed drive the growth of human intelligence over the past three million years. Most evolutionists believe in the Machiavellian theory that bigger brains were needed in an arms race between manipulation and resistance to manipulation. In Rice and Holland's words: "The phenomena we refer to as intelligence may be a by-product of intergenomic conflict between genes mediating offense and defense in the context of language".
However in spite of competition, sexual destinies are inextricably entangled. Two male imprinted genes in mice , Mest and Peg-3 are both involved in good mothering in daughters (p 346). Peg-3 affects neurons that react to oxytocin, inducing lactation and mediating maternal behavior. Mice with defective Peg were slower to build a nest and gather stray pups, losing 9/10ths rather than the normal 2/10ths of their first litters. It is difficult to interpret good mothering in daughters as selectively benefiting male genes.
Sexual selection by the opposite sex, particularly the female is pivotal in evolutionary viability. We need sex to survive, while sacrificing half our genetic endowment to another and suffering the ultimate penalty - mortality - in seeking the variety sex produces. We can ultimately succeed at playing this Prisoners' Dilemma game only through producing viable offspring and in this the investments and strategies of men and women are clearly as different as our haploid manifestation as sperm and ovum. A man's investment can be as small as a few drops of semen, but a woman's is as overwhelming as pregnancy, as needful as lactation and as enduring as childhood. Men marry and sew wild oats, while women seek a resourceful monogamous partner and have secretive affairs. Neither is strictly faithful overall, nor could they be and fully protect their own genetic heritage. There is thus no escape from the paradox of sexual betrayal either, just temporary respite in fidelity and love's sweet embrace. The downfall of the Prisoners' Dilemma game in marital discord, jealousy, divorce, violence and desertion is a frequent cause of murder and suicide.
The sexually paradoxical nature of the mind-body relationship brings with it the implicit risk of 'double jeopardy'. The root of the existential dilemma is to experience consciousness through a physical body suffering inevitable decay and mortality. Yet the physical world and with it our body and sensory organs are our gateway to conscious experience (p 364). In the breakdown of this paradox into conflict comes the notion of light and dark forces and the mortal combat of god and satan. This has led religious thinkers, from the first gnostics, through Augustine, all the way to modern Western culture to perceive conscious existence as a spiritual, godlike self or soul trapped in lustful, fallible, flesh (p 242). A flesh that both condemns us to mortality through its frailty and robs us of our freedom through sexual desire. The penis, which is the source of future life for mankind, then becomes an agent of the devil's work. In turn, lubricious sexual intercourse with demons became a central fantasy in the witch hunts. This degenerate view of sex as evil exploitative lust still pervades Western society's views. It continues to surface in diverse forms of perversion, pornography and prostitution.
Given the universal nature of the Prisoners' Dilemma, it is of little surprise to discover that humans are innately attuned to distinguishing cheating, deceit and betrayal. In many experiments Leda Cosmides and John Tooby have shown that we can far more easily solve a logical puzzle if it is presented as a question of detecting betrayal. To detect proof of unmitigated altruism is far more counter-intuitive. Matt Ridley (R578) illustrates this in the following story. Chief Kiku, who demands his followers are tattooed, tells four hungry villagers "If you get a tattoo on your face you will get a cassava root in the morning". A visiting economist wonders "Will he keep his word?", while an anthropologist, thinking he is bluffing says "Surely he would not refuse food to a man just because he didn't get a tattoo!" Kiku's reply is "Tell me this or I will tattoo your faces myself. The first got a tattoo, the second had nothing to eat, the third did not get a tattoo and the fourth I gave a large cassava root. Now tell me which of them you must ask of to answer your question." This is an example of the "Wason test", which is counter-intuitive as a logical puzzle unless it is presented as a test of breaking a social contract. Three quarters of Stanford students get the answer to economist's puzzle right, but most flunk the anthropologist's test.
The paradox underlying the Prisoners' Dilemma has a kind of physical realization in the form of a 'spin glass - a material in which a set of embedded spins, acting in the same way as molecular domains in a magnet, are coupled by a random, normally distributed linkage. Unlike a ferromagnet, where all the spins line up in one dominant, polarized minimum energy state, a spin glass has a large number of potential energy minima in which cooperation between some spins results in frustration between others. The medium partitions into zones of cooperation punctuated by interfaces of defection. This displays a deep relationship between symmetry-breaking, complexity, instability, and the Prisoners' Dilemma.
The intractable nature of the Prisoners' Dilemma in the 1960s made it a cause celebre in the burgeoning area of game theory in economics. At first theorists believed there was no escape from the implications that the game equilibrium favoured selfishness because the relative payoffs of the strategies of each meant that defection remained a strategic equilibrium for both players. Human generosity thus seemed an aberrant and foolish deviation. But then a new generation of game tournaments set a stage for a more realistic appreciation for a way out. In the first of these, it was noted that real humans playing repeated Prisoners' Dilemma games are much nicer to one another than the single game payoffs would suggest. Knowing the rules of the game they generally cooperated till the end of the tournament when they would stage final defections to secure a terminal advantage.
In the 1970s there came a convergence with evolutionary biology in the form of John Maynard-Smith's concept of an 'evolutionarily stable strategy' - a product of natural selection which would arrive at a game theoretic strategic equilibrium and hence be sustainable in evolutionary terms because no strategy of an opponent could lead to break down of the selected trait. Towards the end of the decade the rise of computers made strategic tournaments possible and the political scientist Robert Axelrod, exploring the logic of cooperation, catalyzed the first strategic answer to the Prisoners' Dilemma. He invited all comers to submit computer programs to a repeated tournament of 200 games. The astounding result was that a simple strategy in the form of 'tit-for-tat', submitted by Anatol Rapoport, another political scientist, with an interest in problems of nuclear confrontation, proved the decisive winner. We all know tit-for-tat in the form of the Biblical invocation of 'an eye for an eye and a tooth for a tooth'. We also know tit-for-tat is forgiving in cooperation, doesn't seek to defect, but punishes defectors by retaliation. However it does have one serious flaw - intractable bouts of revenge retaliation. Following on from this discovery emerged a whole series of challenges in a development of the game in which strategies could compete and proliferate according to their success in the manner of an artificial life experiment. While 'tit-for-tat' was singularly effective at driving out the hawks of defection, even 'nicer' strategies which broke the impasse of retaliation surfaced. Upon his discovery, Axelrod contacted William Hamilton and a further expansion of understanding occurred. Evolutionary genetics was at this time in full retreat from the notion of group and species selection, with the realization that selection was predominantly on an individual, not a species basis, and that it was genes and certain genetic traits which were being selected for, not the welfare of the organism or the species as a whole. Richard Dawkins' notion of 'the selfish gene'(R151), although a clichéd oversimplification, carries a root truth - that it is genes which are being selected, even if the vast majority do so under the constraints of co-residing in a given organism, which must itself survive under social, and environmental, conditions, including running the gauntlets of sexual enticement, and good parenting, shared by a species.
This pendulum has now swung back from the brink of extreme genetic selfishness, in a recognition that group social selection can also play an important role in shaping individual traits. If battery hens are selected for individual laying capacity they tend to compete, become stressed, and not to lay well in cages. However selecting for good laying cages results in socially more compatible chickens which lay better over all. More generally, forms of social selection, from ostracism to violence, do have selective evolutionary effect. Nevertheless genetic selection is the key to the whole mechanism of mutation and selective advantage, so biologists have ever since sought with ingenuity to elucidate ways in which genetic selection could give rise to the altruism we find in human interactions.
A key step was Hamilton's discovery of 'kin selection' - the idea that organisms will evolve not just to preserve and reproduce their own genes but will also invest in the protection of the common genes they share with their relatives and offspring. This relation is neatly expressed in the inequality C < Br , where C is the cost, B the fitness benefits and r the relatedness of the benefited relative. We thus expect raw genetic considerations to favour strategies where an organism will invest around half as much effort in protecting immediate offspring and siblings as in one's own livelihood. A host of examples confirm these principles in nature, from the honey bee to chimpanzees. As Hamilton (R285) put it: "a gene causing altruistic behavior towards brothers or sisters will be selected only if the behavior and the circumstances are generally such that the gain is more than twice the loss ... to put the matter more vividly, an animal acting on principle would sacrifice its life if it could thereby save more than two brothers, but not for less" (Hrdy R330 64).
Robert Trivers (R702) then introduced the wider arena of reciprocal altruism. De Waal (R163 24), in exploring friendship and mutual aid, notes the outstanding characteristics of reciprocation: "Rather than simplifying the relations between genes and behavior, [Trivers' article] pays full attention to the intermediate levels such as emotions and psychological processes. It also distinguishes different types of cooperation based on what each participant pus into and gets out of it. For example cooperation for immediate reward does not qualify as reciprocal altruism. ... Because of the instant payoff, this kind of cooperation is widespread [and could be viewed as mutual self-interest]. Reciprocal altruism on the other hand costs something before it delivers benefits. It has the following three characteristics: (a) the exchanged acts, while beneficial to the recipient are costly to the performer, (b) there is a time lag between giving and receiving, (c) giving is contingent on receiving."
Hamilton was struck by the correspondence of Axelrod's results with Trivers' idea of reciprocal selection. This would require each to punish cheating by reciprocating only with individuals who had fulfilled their part of the reciprocation bargain, and would thus require careful social discrimination and recognition. During the 1980s, field evidence of such reciprocation began to emerge. Vampire bats, who roost together in hollow trees, can generally get more than a meal for themselves if they do score a hapless victim in the night. They can only survive a day or two without blood and roost together so they have evolved an elaborate system of reciprocation to feed their neighbours, who are not necessarily genetically related. They have evolved to vomit excess blood to their co-residents on a reciprocal basis. These 'neighbours' have relatively stable roosting places although they are not necessarily related individuals. Reciprocation requires careful score keeping, rewarding cooperators and punishing defectors. To do this it needs stable long-term relationships without frequent mixing of individuals or the tally cannot be kept. Notably Vampire bats have the largest brains of bats, consistent with the relative complexity of such social discrimination. They also groom one another closely in the stomach region, which could be a giveaway for cheating. African vervet monkeys are similarly reciprocal in getting aid in fights. Cleaner fish on reefs are in a mutually reciprocal relationship with those they clean of parasites, who never seem to take advantage and eat the cleaners. Although this doesn't involve strict reciprocation, it clearly has reciprocal advantages.
However reciprocation is actually quite rare in the natural world, apart from a handful of additional examples from dolphins, monkeys and apes. Miller (R475 301) notes "Evolution appears to avoid reciprocity whenever possible". For example lionesses investigating a potential threat do not enforce reciprocal favours. Some lead the counter-threat and though they may look balefully at their laggardly sisters who slink behind, do not punish them for their cowardice even when it is repeated, or fails when most needed. In many situations, the payoffs may be too indifferent, the populations too mobile and the score keeping too cumbersome to maintain reciprocity. In addition the tit-for-tat nature of reciprocity, as we have noted, leads to intractable cycles of revenge punishment. De Waal notes "this process is evidently a lot more complicated than simultaneous cooperation. There is for example the problem of the first helpful act - a gamble since every partner does not follow the rules. ...Reciprocal altruism does not work for individuals who rarely meet or who have trouble keeping track of who has done what for whom: It requires good memories and stable relationships, such as are found in primates. De Waal then explores the evolution of what we might call 'morality' in "Good Natured" in the variety of mutual 'friendship' behavior in apes based on the similarity principle - contemporary individuals (particularly females) sharing mutual interests in a similar life situation and social ranking.
Game theorists such as Martin Nowak were quick to pick up on tit-for-tat's weaknesses and an artificial life contest ensued between different strategies under a variety of conditions. Probabilistic strategies now came into play which could vary their response a proportion of the time. In addition, learning from mistakes and successes were now allowed to take place. Out of this milieu came new strategic variants which could engulf 'tit-for-tat', such as 'generous', which forgives single defections about a third of the time but rejects them sufficiently to repel 'always defect'. Thus 'turning the other cheek' becomes part of astute Machiavellian behaviour. Among 'generous' players, 'always cooperate' can now thrive, but this again becomes susceptible to 'always defect', resulting in a complex system with no fully effective strategy, leaving a solution to the Prisoners' Dilemma again beyond reach. This cyclic ambiguity caused consternation until 'simpleton', a game originally invented by Rapoport, with a , with a 'win-stay; lose-shift' strategy, called 'simpleton' or 'Pavlov', once discarded because it was a 'sucker' to 'always defect' now proved to be able to trounce 'tit-for-tat' once 'always defect' was eliminated. Essentially tit-for-tat is an extrovert, who does what the opponent did last, and simpleton is an introvert who switches if they get punished. There is evidence for such behaviour in nature. In the alternate leading and following of stickleback scouting parties testing the reaction of predatory pike, which superficially looks like tit-for-tat reciprocation, the scout fish will alternate between defection and cooperation, when faced with persistent defection.
Various forms of the Prisoners' Dilemma game can be played as cellular automata, (p 510), which display complex punctuated equilibria between defectors (black), cooperators (red), tit-for-tatters (purple), 'simpletons' using win-stay lose-shift (green) and random strategies (cyan) (ex. Flake R213). Players on the grid play in pairs for several rounds and then each cell adopts the most successful strategy in its neighbourhood. The top row shows the 1st, 2nd, 5th, 10th and 50th tournaments. An initial wave of defection is taken over by reactive strategies. The system stratifies in a state dominated by tit-for-tat and 'simpleton' with a few islands of cooperators and the odd defector. The bottom row includes 10% mutation and noise and is in dynamic flux. Such interactions can help explain how reciprocal altruism can emerge without complex memory, if nearest neighbours remain stable, for example because of fixed territories in a given habitat (Nowak et. al. R506, R510).
By introducing alternating moves, as in reciprocation, Marcus Frean (R786) established 'firm-but-fair' as a winning strategy. Like 'simpleton', this cooperates with cooperators, returns to cooperating after a mutual defection and punishes a sucker by further defection, but it also continues to cooperate after being the sucker in the previous round. This accords with the common sense of giving a good impression if you want others to act in your example. Even lowly guppies have complex scouting strategies, preferring reliable colleagues in scouting parties, ostracizing laggers, and being more tolerant of defections in consistent cooperators. Grim (R270) has noted that the sequence of such strategies results in the ultimate winner of the Prisoners' Dilemma becoming an undecidable proposition (p 491).
A prisoners' dilemma game set generated to illustrate one can afford to be kind and turn the other cheek out of tit-for-tat a quarter of the time and survive under a spread of payoffs (centre standard game) Red is always cooperate, green 'simpleton' or Pavlov i.e. stay unless the other guy punished you last time in which case swap, purple 'tit-for-tat' i.e. do what the other guy did last, cyan 'firm-but-fair' (tit-for-tat with 25% turning the other cheek to encourage cooperation), and black outright defection. Depending on the payoffs for CC (wine and roses), CD (beaten to submission) DC (ultimate victory) and DD (double jeopardy), under a regime of noise and some mutation, we get different populations. The images go 3 0 4 0, 3 0 4 1, 3 0 5 1 (the standard payoffs), 3 0 6 1 and 3 0 6 2 each at the 25th 5-game tournament round. Firm-but-fair is usually defined in an alternating, rather than simultaneous play-off, game. Tit-for tat will eventually dominate in the right hand-game with defection coming number 2.
Prisoners' dilemma games can readily be played as cellular automata (p 510), leading to complex and punctuated equilibria. Nowak et. al. (R506) have run such competitions with genetic algorithms for mutation and natural selection of strategies for millions of generations. Outcomes even for fixed automata may become formally undecidable (p 491) because they can only be modeled by a computational simulation.
Of course, in a real world, defection is the 'criminal' element that can never be fully eliminated once and for all. Mutation and selection are always throwing up such strategies in evolution in a manner which can never be eliminated. Parasites and disease are an inextricable part of the tooth and claw of the evolutionary endowment. Furthermore the realities of population movement allowing cheaters to drift to new victims and the varying payoffs each life situation provoke make it difficult or impossible for any single strategy to prevail. The ineradicability of defecting strategies is as signal of human society as it is of the evolutionary paradigm. Most people will learn to take advantage of flagrant opportunities foolishly presented. While criminality can be contained through a mix of penalties and good social policy, only in a naive world would it be expected to disappear entirely. Moreover in real situations, rare strategies often invoke equally high payoffs which guarantee no escape. In a promiscuous society of deceiving whores, a single faithful wife can command a king's ransom and will become at an inestimable advantage reproductively. By the same token in a monotonously monogamous society, a single scarlet woman can command the affections of every man to the highest station. Evolutionary geneticists comment that for this reason, pure genetic monogamy is not an evolutionarily stable strategy, always liable to invasion by 'fast' females and 'philandering' males. Thus the real games of life often tend to an equilibrium between cooperating and defecting strategies, making the Prisoners' Dilemma a permanent feature of natural and social survival. The Red Queen evolutionary arms race between parasites and prey is likewise a perpetuating prisoners dilemma, giving high enough payoffs to maintain sexuality, despite the halving of each parent's genetic endowment.
In mammalian evolution we also have the emergence of emotions and the effects of emotional reactions on the whole question of genetic determinism, selfishness and altruism. Rather than following instinctual or imprinted genetic strategies, mammalian brains have evolved a meta-strategy providing an emotional spectrum of reactions, from flight to fight, from love and close intimate bonding to hate, and the violence of hunting play, within which the direct simplicity of kin and reciprocal altruism become a complex emotional dynamic only partly genetically based. Instances abound, not just of seemingly irrational human generosity, which cannot be interpreted to benefit the individual directly or indirectly, but irrationally altruistic emotional reactions of mammals. A hippopotamus may repeatedly rescue a wounded gazelle from an alligator, or a lioness raise a young ungulate. We need to explain how evolution could have arrived at such an indirect emotional process as a universal win-win, given the raw constraints of natural genetic selection.
Even in human society, where we have large brains, and abundant capacity to detect cheating and punish defection, neither kin, nor reciprocal altruism, fully explain our behaviour. In differing circumstances, we may retaliate like the vampire, or endure laggards like the lioness. We also have an innate capacity to respond to the plight of others, who may be unrelated, or not even of the same species, with acts of compassion, for which no reward can be gained, or expected. Although human societies have imposed Draconian punishments for criminal defection and sexual betrayal, our life relationships are motivated by the unbounded quest for love and belonging as by astute judgement of character.
A good indication of the degree to which human societies respond to the general issue of egalitarian cooperation comes from the ultimatum bargaining game, where a player is offered a financial reward which they can keep only if they give sufficient to a second player for them to accept the bargain. The second player thus receives either the offered portion, or nothing if they refuse and one might expect them to accept only a small portion. However they also know the first player will receive nothing either if they do so they can quickly punish for perceived 'cheating' on a fair bargain. Even when players play anonymously, so do not suffer a retaliatory round, the experienced players in many cultures from Los Angeles (48%) to Yogyakarta and Tokyo (45%) end up offering only a little less than half - with the most frequent amount being a half share, reflecting the keen eye humans in many cultures have for not accepting a second-class treatment. The people of Jerusalem were a little more stingy at 36% and the Machiguenga of the upper Amazon were a notable exception, offering only a meagre 24% of the booty (Henrich R307).
In the Dictator game, the proposer simply divides the sum between the two players and there is nothing the respondent can do about it. With no fear of reprisal, the proposer makes a far stingier offer. The offer still tends to be more generous than it has to be, because the proposer worries about getting a reputation for stinginess that could come back to bite him in the long run. We know this because of the outcome of the Double-Blind Dictator game, where proposals from many players are sealed and neither the respondent nor the experimenter knows who offered how much. In this variant, generosity plummets; a majority of the proposers keep everything for themselves (Pinker R544 256).
Another game which aptly demonstrates tendency to a winning defection by a dominant group and has major implications for first past the post election, majority democracy and the consequent 'tyranny of the majority' is illustrated as follows. Seven people are given anonymous numbers and connected by computer network. If they are asked to reach consensual agreement to gain a reward, they will negotiate to do so. However, if they are told simply to find a majority to get the reward, they will quickly engage the minimum number of four at random or by pattern, e.g. 1,2,3 and 4 or 1,3,5, and 7, and go straight for the booty, cutting the other three out of the bargain. Majority 'defection' against the whole becomes the rule.
In the 'public good' game, everyone makes a voluntary contribution to a common pot of money, the experimenter doubles it, and the pot is divided evenly among the participants regardless of what they contributed. The optimal strategy for each player acting individually is to be a free rider and contribute nothing, hoping others will contribute something and he can get a share of their contribution. Of course, if every player thinks that way, the pot stays empty and no one earns a dime. The optimum for the group is for all the players to contribute everything they have so they can all double their money. When the game is played repeatedly, however, everyone tries to become a free rider, and the pot dwindles to a self-defeating zero. On the other hand, if people are allowed both to contribute to the pot and to levy fines on those who don't contribute, conscience doth make cowards of them all, and almost everyone contributes to the common and profitable good (R544 257).
Left: Real play in the prisoners dilemma game between pairs of women involves high levels of mutual cooperation until the last few rounds. Right: Play against a computer engaging tit-for-tat results in reciprocal defection (R583).
People do more for their fellows than return favors and punish cheaters. They often perform generous acts without the slightest hope for pay back, ranging from leaving a tip in a restaurant they will never visit again to throwing themselves on a live grenade to save their brothers in arms. Trivers, and economists Robert Frank and Jack Hirshleifer, have pointed out that pure magnanimity can evolve in an environment of people seeking to discriminate fair-weather friends from loyal allies. Signs of heartfelt loyalty and generosity serve as guarantors of one's promises, reducing a partner's worry that you will default on them. The best way to convince others that you are trustworthy and generous is to be trustworthy and generous. Indeed many players of the prisoners dilemma game choose to cooperate consistently until the last few rounds and altruistic punishing of defectors even at high cost to the perpetrator is another paradoxical sign of 'moral' defection for the common good.
Simple virtue cannot be the dominant mode of human interaction or we could dispense with the deliberate financial and legal processes designed to keep exchanges fair and base our economy on the honor system. At the other extreme, people also commit acts of outright treachery and deceitful or criminal exploitation. Machiavellian traits are a central part of human nature, with most people displaying mixtures of, pure generosity, reciprocity and expedience (R544 259). Brain experiments (p 377) have verified that the common emotional basis of both cooperation and altruistic punishment stems from anticipation of social satisfaction associated with pleasure - hence the term 'revenge is sweet'.
We thus need to look more deeply for sources for the natural goodness we associate with social altruism, emotional bonding and human agreeableness and love. It is here that Geoffrey Miller's ideas of sexual selection (p 53) come into their own. Miller notes that all forms of social selection are weak and indirect by comparison with the inescapable powerful positive feedback provided by sexual selection. Every organism has to both survive and reproduce to run the evolutionary gauntlet. To reproduce, we must pass the test of mating selection by the opposite sex, a positive feedback process with capacity for runaway and complexity. Furthermore it is in sexual selection that detecting cheating comes to the knife edge of betrayal, requiring genuine indicators of fitness such as the peacock's tail, the male guppy's orange stripes, and with it, human generosity in love. In Miller's terms the complexity of human society is a product of such fitness indicators, elaborated in response to runaway discerning partner choice, and along with it our innate capacity to detect cheating, while retaining a generosity of heart necessary to entice the other sex into choosing us as worthy mates.In conceiving the complexity of human society and its teeming Prisoners' Dilemmas of social coexistence and competition, sexual paradox thus remains central as the gateway through which all our intellectual and cultural pretensions go down the plug hole to the next generation. It is also our heart centre, our raison d'etre motivating our passion and our jealousy in a way which all the other panoply of social interactions from hard nosed business to internecine strife serve as a resourceful backdrop. We thus need to strike a creative balance between the dictates of reciprocation and its manifestations in social game theory and sexual selection as a generator of cultural complexity.
The Prisoners' Dilemma does not have to lead to dissonance and a war of attrition. It its fully contradictory form, the paradox it contains leads to sexual interdependence and climax diversity. The fulfillment of sexual paradox is constructive engagement with the opposite sex in choices which abet successful child rearing, trading off the nemesis of deceit and betrayal with the sexual freedom of choice each gender must needs retain to fulfill their own reproductive design. The solution to the existential Prisoners' Dilemma of conscious existence is likewise constructive engagement with the living universe, through realizing love in the passage of the generations, assuming personal responsibility for ones willed actions and their cumulative affect on the future world around us. This is essentially the sustainable reproductive solution - evolutionary sustainability. But it is also the psychic resolution in mature interdependence, rather succumbing to mutual defection in the face of the win-lose strategies of submission and dominion, with their consequent tragedy of planetary destruction and the loss of future quality of life for the generations to come.
The success of reality TV shows such as "Survivor" depend on human interest in Machiavelian strategies in a Prisoners' Dilemma trial in which one person from a group wins a million dollars in a succession of eliminations in contests and tribal councils in which coalitions and betrayals are climaxed by a final vote of the eliminated members for the victor.
Many of the crises and tragedies of human 'civilization' arise from the loss of sexual paradox through prisoners dilemma betrayal by one party or another, leading to a degenerate process of domination, exploitation and atrophy. Rather than coming to the conclusion that humanity is a sick or dangerous species, which through its implicit violence poses a threat to the future of the living planet, our answer here to these maladies will be to restore the state of sexual paradox and with it our evolutionary and cultural sustainability as a species.
'Don't get even, get mad': Why Emotions Matter
Studies of brain function attest to emotional responses being central to how humans respond to issues of fidelity, and deceit, trust, cooperation altruistic punishment (p 378) and revenge (p 391).
Attempts to make game theory applicable to real life date back to the 1950s, when mathematicians used it to advise the US Air Force on Cold War strategy. Even then, it was obvious that most real-life problems aren't remotely like zero sum games where what is good for one is bad for the other and in which game theory recommends choosing the highest scoring tactic in the worst situation. What is bad for one 'player' can often be equally bad for the other, as the Prisoners' Dilemma shows. A classic is the game of Chicken, immortalized in James Dean's 'Rebel Without a Cause'.
As with zero-sum games, there's a rule for finding optimal strategies for these more complex games, which won RAND mathematician John Nash a share of the 1994 Nobel Prize for Economics. Nash's theorem says that it is possible for a player to choose a strategy that is best for him or her when all the other players are also following their best strategies. In this 'equilibrium', no player can improve his or her prospects by choosing an alternative strategy. But there is no single state of equilibrium for a game like Chicken. There are two: you can decide to swerve, while the other person plans to keep driving, or vice versa. In either case, neither you nor your opponent can improve your score by unilaterally changing your mind, reflecting the cusp catastrophe's two states (p 14).
Enter the role of emotions. Only truly irrational players can credibly threaten to drive on no matter what - and so a rational strategy is to be completely irrational. Such 'paradoxes of rationality' dogged game theorists through the 1970s and 1980s. A huge effort was made to find rules for selecting the most 'rational' strategy in every game; none really worked. Nigel Howard, a veteran game theorist who had advised the US government in the Strategic Arms Limitation Talks during the 1960s was well used to applying game theory in real-life situations - and well aware of its limitations and called a meeting of game theorists at Sheffield University in 1991 in which 'drama theory' or 'soft game theory' was born (R450). He points out that the effects of rationality can be dire, recounting the following story. Two economists are taking a taxi to their hotel in Jerusalem. Worried that they are going to be overcharged, they decide not to haggle about the price until they reach the hotel. But the driver is so outraged at their conduct that he locks the taxi doors, drives them back to where they started, and dumps them on the street. "What we were really dealing with here weren't just games," recalls Howard. "They're dramas, where the beliefs and values of the characters evolve as the plot unfolds." At its heart is the idea that games are not static, one-shot deals decided by rationality, but dynamic situations that can be utterly transformed by the emotions of the players.
During the 1960s, Howard himself had developed 'metagame theory', which focused on the role of paradoxes in determining the outcomes of games. In the game of Chicken, for example, it seems pretty rational for Jimbo to want to win. Yet to do this, he must convince Buzz that he will not swerve, no matter how much Buzz insists he won't either. But coming from a rational person, Jimbo's threat is hardly credible: no sane person would declare a determination to follow hell-bent Buzz clear off the edge of the cliff. There's a way out of this 'credibility paradox', however: Jimbo should stop acting rationally, and instead behave as if he is crazy before he goes anywhere near his car. Suddenly, his threat to keep on driving becomes all too credible. Irrational behaviour thus sometimes pays, although it seems to be more to impress male mates and become a popular hero than to directly impress the girls (p 55). Howard has showed that the idea of credibility paradoxes gives a firm mathematical basis for drama theory (R328). "The basic idea is that paradoxes have an emotional effect on the characters and the reason these emotions emerge - like anger and fear, or affection and goodwill - is that they have a drama-theoretic role. They shake the characters out of old ways of thinking, allowing them to see a new way forward."
Chicken involves an 'inducement paradox', in which Jimbo must use an irrational threat to induce Buzz to swerve. Others, including the Prisoner's Dilemma, involve a 'cooperation paradox'. For each prisoner as an individual, Nash's theorem gives a unique, rational solution: accept the police offer, and start talking. But for the pair as a team, both spending a month in prison is preferable to one being locked away for years. But the only way of achieving this is for both prisoners to put their trust in each other and stay silent. This creates a cooperation paradox: each must convince the other that they will act as a team despite the fact that each could do better for themselves by defecting. For long-standing partners in crime emotional bonds will come to the fore when they face the cooperation paradox. But if one of the prisoners has always been an unwilling accomplice, the cooperation paradox will trigger anger and distrust and he'll act to save his own skin.
The Red Queen on the Origin of Sex
In "The Red Queen" (Ridley R577) explains the origin of sex (p 334) in a way which makes it effective, even in a single generation, despite losing half the genes transferred to the next, an acid test for the process having evolutionary stability at the outset:
"Sex is not about reproduction, gender is not about males and females, courtship is not about persuasion, fashion is not about beauty and love is not about affection. It is about getting your genes into the next generation, and trumping the Terrible Three: predators, parasites, and the neighbors. Of that trio, parasites rank as the greatest foe."
The idea is that sexuality evolved from an immediate potent advantage in the first generation that results from confounding parasites and predators because of genomic diversity that results from sexual recombination (p 329). Parasites and hosts are locked in a genetic arms race in which sexuality provides a potent advantage in generating variety, making it difficult for a parasite to adapt to varying individual hosts. It gives the clearest and most powerful explanation for the widespread occurrence of sex in higher organisms. There has to be at least a twofold advantage to make up for transmitting only fifty percent of our genes per generation sexually rather than the hundred percent transmission in parthenogenesis. It answers the bootstrap question in a way which doesn't makes sense otherwise. Although we now know that sexual recombination is a powerful source of variety, enabling complex organisms to evolve, this goes no way to explaining how the process could get going in the first place. It's really no use trying to explain this in terms of an evolutionary advantage of greater adaptability if this only emerges very gradually in the long-term over a large number of generations. We need a powerful immediate effect in the first generation, otherwise sexual game theory will say we still have a better chance of survival to invest all our genes in parthenogenesis than only half in a sexual exploit that would take up to a hundred thousand years to come to fruition. We would all die waiting, swamped by our parthenogenetic predecessors. The answer to this is that sex provides an immediate answer to the epidemic cataclysm awaiting a parthenogenetic organism when parasites or diseases adapt to a single genotype. The Red Queen is thus the 'scarlet woman' in sexual evolution. A similar one-generation advantage will accrue if an organism is subjected to any form of stress which compromises survival of daughter offspring of the current clone (p 336).
The "Red Queen" hypothesis has itself evolved historically through a sequence of based on coevolution. The original idea is that in tightly coevolved interactions, evolutionary change by one species (e.g., a prey or host) could lead to extinction of other species (e.g. a predator or parasite). Van Valen (R715) named the idea "the Red Queen hypothesis," because, under this view, species had to "run" (evolve) in order to stay in the same place. The next idea is that coevolution, particularly between hosts and parasites, could lead to sustained oscillations in genotype frequencies (Bell R54). In species where asexual reproduction is possible, coevolutionary interactions with parasites may select for sexual reproduction in hosts as a way to reduce the risk of infection in offspring. The idea of the Red Queen hypothesis as a founding strategy leading to sexuality has been given a compelling case by Ridley (R577).
In Alice's dream (Carroll R109) about the looking glass house, she first finds that things appear left-to-right, as if shown in a mirror. She then finds that chess pieces are alive. Alice decides that it would be easier to see the garden if she first climbs the hill, to which there appears to be a very straight path. However, as she follows the path, she finds that it leads her back to the house. When she tries to speed up, she not only returns to the house, she crashes into it. Hence, forward movement takes Alice back to her starting point (Red Queen dynamics), and rapid movement causes abrupt stops (extinction). The flowers tell Alice that someone like her often passes through, and Alice decides to seek the Red Queen. She begins moving toward her, but, the Red Queen quickly disappears from sight. Alice decides to follow the advice of the rose: "walk the other way". Immediately she comes face-to-face with the Red Queen (Lythgoe and Read R429). Already, in this world, straight can become curvy, and progress can be made only by going the opposite direction; now, according to the Red Queen, hills can become valleys and valleys can become hills (a peak in a sexually reproducing host population leads to a coevolutionary peak in parasites and a subsequent valley in the hosts). At the top of the hill, the Red Queen begins to run, faster and faster. Alice runs after the Red Queen, but is further perplexed to find that neither one seems to be moving. When they stop running, they are in exactly the same place. Alice remarks on this, to which the Red Queen responds: "Now, here, you see, it takes all the running you can do to keep in the same place". And so it may be with coevolution. Lewis Carrol's Red Queen is running while standing still, just as we end up as sexual species running while standing just about still with respect to our parasites and diseases in a paradoxical arms race with no final resolution. Evolutionary change may be required to stay in the same place. Cessation of change may result in extinction. We may find it hard to accept that we are evolving and evolved sexuality just to evade our parasites, but we nevertheless acknowledge that parasitism and infectious disease is a principal cause of death, even in the age of modern technology.
A basic feature of both immune system genes and the histocompatibility genes that make each individual's tissue unique is the existence of a large library of variant genes in individually unique combinations. A single mammalian species contains over a hundred different histocompatibility genes. The immune system is even more complex combining the effects from several light and heavy chain gene libraries and further induced mutations at the variable binding site, to generate millions of different antibodies. Sex acts as an agent to promote the diversity required to evolve such libraries. It also recombines them genetically each generation in a way which makes it difficult for pathogens to adapt to more than one generation of host. Sex gives a doubly powerful first-generation advantage because the descendents of each individual have both different immunity and different idiotype.
An outstanding example, which illustrates the dynamic nature of intermittent sex occurs in freshwater snails in Africa which are hermaphroditic in a self-contained way. Whenever the nematode parasite Bulinas truncatas strikes with the rains, the snail responds by growing penises and sexually recombining (Blum R66 8). In many species, evolution of sexual genes is very rapid as a result of a Red Queen arms race between male and female. This is true of the abalone, where the sperm secretes lysins which dissolve the egg membrane admitting parasites, so there is a genetic immunity arms race between the egg and the sperm (Jones R349 133). It is also true of the human Y chromosome where maleness genes are evolving rapidly. Ursula Goodenough also sees in such rapidly evolving sex genes the capacity to induce speciation, and believes this is happening between the Cuban and American ocean populations of the single-celled alga Chlamydomonas (R66 11). Likewise social patterns of promiscuity in higher apes are reflected in increased rates of evolution of the SEMG2 gene which makes semen thicken after ejaculation (R771).
There are intriguing indications of an arms race in humans between sperm production and cancer resistance. The genes most rapidly evolving between humans and chimps are immune defense genes - a classic Red Queen race between parasites and hosts, and cell apostosis genes programming cell death. Protection against cancer resulting from apostosis may compete with the need for sperm to evade apostosis in competitive reproduction (Nielsen R502). There is a similar evolutionary arms race in the SEMG2 gene coding the thickness of semen correlating with promiscuity in differing ape species (Wyckoff R771).
The result of sex is profound. Once established, sexual recombination makes possible the most powerful means of creating genetic diversity known. Genetic crossing-over in meiosis and the careful sorting of the DNA this entails (p 329), enables a precise and complete genetic combination of the genes of each parent, crossing the sister alleles so perfectly that virtually every sexual offspring contains a fully viable genome when the sex cells merge again in fertilization. It is this almost endless variety and the powerful selection it provides that has made the evolution of higher organisms possible. Hence all higher organisms have evolved from sexual species and the vast majority are obligately sexual.
Species which have both sexual and asexual reproduction tell us a lot about what causes the equilibrium to shift between the two. Asexual reproduction is good at rapidly multiplying to invade a habitat, as with aphids and vegetative reproduction of the Nile lotus. In the freshwater minnow Pocillopsis asexual individuals are good at populating extreme environments, where sexual recombination would dilute adaptive characteristics. But sexual individuals are better at populating varied, fluctuating and evolving environments.
Sexual recombination has the capacity for eliminating undesirable mutations which are continually accruing, by concentrating them in only some offspring, where natural selection can effectively eliminate them - a process cryptically called 'Muller's ratchet'. If we reproduced clonally, all our offspring and their offspring would inevitably suffer the random mutations of entropy. Selection cannot necessarily keep all these in line and prevent gradual degradation of a complex genome, despite selection unless there are some forms of recombination as insurance of error protection. We already have sophisticated error-correcting enzymes which read off one strand of DNA to correct the non-complementary or damaged bases on the complementary strand. But even these processes cannot distinguish which strand is a mutation and which is the original, so error correction also involves keeping and comparing variants and allowing these a chance of survival. If we are sexual beings, our children each contain half our genes in a unique combination. If each of us have only one or a few mutations at the tolerable load per generation, some of our children may have two mutations but others will be free of any. This ensures some individuals are carrying unmutated genomes. Lynn Margulis has suggested that a similar error-correction process may have driven bacterial pan-sexuality. Notably asexual rotifer species have a much smaller load of transposable genetic elements (p 331) consistent with a mutational basis for sexual recombination. For eucaryotes existing before life generated the oxygen atmosphere and the protective ozone layer, a solid reason for sexual recombination, again consistent with the Red Queen, would have been to protect the genomic information of small exposed single-celled organisms from the ravages of ultraviolet mutagenesis.
The Red Queen hypothesis also naturally leads naturally to a partially competitive genetic and evolutionary race with the opposite sex, an amatory arms race, genetically interdependent, yet with conflicting reproductive strategies and modes of genetic selection. These arms races are evident in the natural world. A male fly may introduce toxins into the female which cause her to invest more energy in the current offspring than her natural investment spread evenly among all her offspring, thereby maximizing her investment in his offspring (p 16). These have other effects, reducing the females capacity to eject sperm and her capacity to mate successfully with other males. She responds by developing immunity. Repeated fertilization can become poisonous to the female. The Red Queen can thus be extended directly to the genetic arena in the form of 'interlocus contest evolution' between competing genetic influences, for example antagonistic genetic selection between opposing sexual characteristics in males and females, characteristic of sexually antagonistic co-evolution.
A stunning extreme of this conflict between the sexes occurs in the little fire ant, where the haplo-diploid sexuality where workers are produced by normal sexual reproduction, but daughter queens are clonally reproduced. Although clonal reproduction increases the queen's relatedness to reproductive daughters, it can potentially reduce the male reproductive success to zero. To compensate the males have also evolved to reproduce clonally from father to son in a sexual standoff, probably by expelling the maternal chromosomes, which leaves their gene pools entirely separate and selected only through the workers although it remains possible that males may occasionally mate with a top queen (R219).
The Red Queen is an instance of the Prisoners' Dilemma. Both parasite and host and male and female are running a treadmill in evolutionary terms while standing still in an arms race from which in the case of the sexual arms race neither party can escape.
Sexual Selection, Reproductive Fitness and Sexual Paradox
"The idea that females are discriminating and can actively choose with whom to mate was controversial from its inception - perhaps because male-male battles can be quite spectacular. ... In comparison female choice is much more subtle. Over the past 25 years, a considerable body of evidence for female choice has accumulated. Females actively choose their mates in a large variety of species." (Dugatkin and Godin R177).
Even 'lowly' guppy fish display a complementation of genetic 'nature' and social 'culture' in female reproductive choice. Although female guppies prefer larger, brighter orange, daring males who closely explore predators, a test of both their metabolic (carotenoid pigments are costly to make) and physical fitness and alertness, they will also follow a previous female's choice in 'social copying', and favour a less-orange mate, provided the differences in orange colouration between two males are less than 25%. However if a female is living under genuinely threatening conditions, she may prefer to mate with a less showy male who provokes less direct risk and genes which carry this lower risk. Her sexual choices are thus a subtle mix of genetic and social and involve both natural and sexual selection. Although people are more complex than guppies and lekking sage grouse, the same mate-choice rules apply to human mating. According to popular wisdom, it is human females who are the choosier sex when it comes to selecting a mate. As a species, humans meet the criteria for female choice: men for the most part, will avoid fighting to the death for the hand of a maiden. And females distinguish between various males on the basis of their characteristics.
Sexual choice can lead to runaway sexual selection, particularly in birds, which have flashy males partly due to the ZW sex chromosome system (p 342). The peacock's tail is a genuine indicator of fitness because, although mesmerizing to females, it makes the peacock vulnerable to predators. There is a runaway selection happening here between the peacock's tail and the choosy genes of pattern discrimination in the female brain. Song birds have partially evaded this penalty by choosing ultra-violet markings. Birds have four colour vision, but song birds push one colour receptor up into the ultra-violet where mates see it stands out but out of the visual range of predatory birds which use a lower wavelength receptor (R14). Sperm are a scarce resource which invites sophisticated social strategies. Male fowl devote considerably more sperm to their first encounter with a new mate than with a familiar one. They will also increase sperm if rival males are around. An attractive hen with a large comb will receive more sperm. Cockrels will even seduce regular partners with sperm-free mountings which trick the female into fidelity even though they would expel the sperm of an inferior mate within seconds of copulation (R547, R548).
Humans are no exception to the rule that variance in reproductive fitness is greater in males than in females. While a significant number of males have no children at all, a few sire hundreds or even thousands of children. In biological terms, humanity is moderately polygynous, regardless of cultural mating systems. It holds as true in serially-monogamous America as it does in polygamous Africa.
The sexes are intrinsically polarized in their reproductive investments (p 334), with females contributing cytoplasmic eggs and the males only contributing DNA, becoming the 'sneaky' sex (p 335). Females can bear offspring by any fertile male, but males must compete to fertilize females, or their larger less abundant eggs, to reproduce. This greater female investment tends to make the female more choosy about her mate and gives female sexual selection a primary role in sexual evolution . This polarization is extreme in mammals, where internal fertilization, gestation, live birth and lactation cause the female investment to be maximally different to the male. It is particularly true of the human female with her vulnerable enormity of pregnancy (p 84). Trivers (R703) first laid out the impacts of the differing investments made by males and females in reproduction and their consequences for sexual selection (Hrdy R330 37). Mating investment has a large fixed cost to succeed at all, so males tend to invest primarily in mating, tending towards competitive polygyny (Low R427 42), while females invest primarily in parenting. Males thus look for reproductive value in females, while females look more to resourcing value.
At an extreme of choosiness, female Californian fiddler crabs, Uca cernulata, will investigate up to 100 male burrows, beckoned inside by the males' large waving claws, to find a burrow of just the right size which will hatch their progeny just in time for them to be spread by the peak outward night time flow of the bi-weekly tidal cycle.
Measures of polygyny are biologically related to the differential variance in reproductive efficacy which is generally higher in males. The means of the two are always the same since it takes a male and a female to reproduce sexually. Thus by biological measures human societies are moderately polygynous, even though we are predominantly socially monogamous. This manifests in a variety of ways. 85% of human societies permit polygyny and in these about as many males as can resource two partners at once do so. Some males engage despotic sexuality. Moulay Ismail the Bloodthirsty of Morocco had 888 offspring and 40 sons in a single month (Hrdy R330 84). Ghengis Khan's Y-chromosome occurs in about one in 200 people as a result of several generations of polygynous descendents and 1 in 12 Irish men are descended from Niall of the Nine Hostages. Wandering males seducing women also contribute, through the standard mammalian strategy of simple sexual courtship. Although we call many human societies 'monogamous' this is clearly a biological misnomer. Most societies with one-spouse-at-a-time rules are called polygynous in a biological definition: more men than women fail to marry, and more men than women remarry after death or divorce, producing more offspring in these later unions. The most reproductive men have many more children than the most fertile women. All of these phenomena increase the variability of men's reproductive success compared to women's, making us polygynous by a biologist's definition (Low R427 54).
The larger divergence in male reproductive opportunity in humans at first caused sociobiologists to concentrate on male evolutionary selection by females, assuming females all reproduced close to the maximum feasible rate. Sarah Hrdy (R329) in "The Woman that Never Evolved" set out to correct this anomaly, noting that real reproductive differences and competition exist in females, particularly in the central issue of successful parenting.
On the other hand, female choice also implies that females will not necessarily remain faithful to a socially monogamous pair bond. A female in socially monogamous species which seek paternal support will seek a resourceful partner but also engage other sexual liaisons in up to 20% of her sirings. Females in polygynous species with dominant males also covertly seek non-alpha partners. This pattern of female 'infidelity' is as true for colonial birds as it is for humans. The principal reason is as insurance so her large parental investment in eggs and in mammals pregnancy and lactation are not entirely bound up in an inferior set of genes. However there are more complex reasons. Females need not just to find a male with the best genes but the most compatible complementarity to hers. Smells of MHC histocompatibility proteins give mammals sensitive indications of sexually attractive mates with good immuno-complementarity. Females also mate with many males to confuse paternity and invite more paternal support and less infanticide. Finally they may mate with non-alpha males to avoid being forced into a undesirable decision by the forces of male competition
Trivers and Willard (R704) went on to establish the relation between such variation and sex ratios: "wherever variation is greater in reproductive success for one sex than the other, and where the reproductive success of individuals of that sex depends on maternal effects, then mothers in good condition should favour the sex with the greatest variance in reproductive success". It has been confirmed in species as diverse as deer, baboons and rodents. Broadly speaking, we expect mothers in poor condition to have more girls and those in good condition to have more boys, possibly mediated by hormonal mechanisms such as testosterone (Grant R254). Women who expect a long life (and are thus likely to be in good condition) have more boys (Johns R341) and Gibson and Macey (R238) showed that rural Ethiopian women with low levels of nutrition are more likely to give birth to girls (p 97). It applies also to human dowry and bride price, where low ranking families save for a dowry to 'marry up' daughters and high ranking families favour only sons and may kill their infant daughters (p 286). Such 'hypergamic' marriage patterns become pronounced under conditions of environmental stress, where upper class families are better protected against famine and can afford males, while lower class families may starve (Low R427 70, Hrdy R330 338) and whose best reproductive prospects over time involve 'marrying up' daughters, in what is called hypergamy.
The rule applies when sexual selection, (access to females) is the dominating factor, but may be reversed when other factors, such as female dominance limit resources. When daughters remain within the group and resources are scant, as in savannah baboons, high ranking mothers produce daughters, but low ranking ones sons who can at least migrate (Hrdy R330 333-5). When daughters can be harnessed for allo-parenting, this advantage can determine the sex ratio, as in Seychelles warblers. Such sex imbalances tend to return to Fisher equilibrium of equality (R212) when the driving factors are mitigated, because the rarer sex gains a strategic advantage. Each sex thus has its own distinct and often conflicting strategy of reproduction. To fulfil a given sex's reproductive imperative requires also fulfilling the reproductive strategy and choice of the opposite sex. Male competition is subject to the paradox of female reproductive choice because it is the most powerful agent of sexual selection in most species. Even in species with pronounced male conflict, female choice remains a prominent selector of male fitness.
Sexual selection is prone to runaway feedback, as for example the outgrowth of the peacock's tail as a genuine indicator of fitness which can't be faked and imposes a significant cost on the bearer in terms of predation. This in turn is driven by the ever-more-choosy retinas and visual areas of the peahen. The balance of these forces and the actual state of strategic advantage one or other sex enjoys varies from species to species. For example in non-monogamous birds where the male contributes only his genes, the prominent display of the peacock's tail and the bower bird are driven by precocious female sexual selection. To be a genuine indicator of reproductive fitness these ornaments are often chosen to be costly, as the peacock's tale is, as well as being a sensitive indicator of highly tuned developmental symmetry indicative of good genes. Experiments have shown that females in displaying avian species will continue to prefer artificially enhanced ornaments and mate with males possessing them confirming runaway selection. The male has little choice here but to make the best job of capitalizing on its runaway evolutionary burdens, which may give it a good chance of siring offspring, but bring costs in vulnerability to predators as a bulky and garish genuine indicator of fitness. This is partly a reflection of the minimal investment made by such males and the incapacity of the males to monopolize female reproduction except through enticement.
Human beauty is has been found to be linked with more perfect symmetry, and mor erecently in an experiment reducing dancing performances to identical computer mannequins, it has been found that, the best dancers are also those who are the most symmetrical and beautiful (Brown R91). The effect was stronger for women watching male dances than for men watching women and the dances performed by men scored more highly overall than those by women, consistent with male display of fitness and female choice.
Even alpha males, who would prefer to engage male competition to win a harem, rather than submit to female choice, find themselves subject to genuine indicators of fitness. An alpha male gelada baboon has a highly visible red chest mark, which indicates his condition. This is probably a sign that also tells others that females are sexually bonded in a way which will be harder to break into. Coalitions of bachelor males will confront a leader of a harem and try to take it over only if his genuine indicators of fitness are lacklustre.
In monogamous species which have mutual mate choice, pronounced sexual differences of display are reduced or non-evident, however as Darwin noted mutual mate choice can still drive selection and consequent evolution, albeit without such strong or polarized sexually selective forces operating. Humans are mildly sexually dimorphic, with testicle size and sperm competition suggesting pair-bonding in a climate of moderate polygyny with mutual mate choice skewed somewhat towards female reproductive choice. Male reproductive variance is greater than that of females. Sexual strategies are complex and mixed with a considerable number of medium to long-term pair bonds, a minority of polygynous associations, serially 'monogamous' partnerships which tend to favour male reproductive polygyny, overlaying a shifting pattern of covert female affairs and sometimes blatant male philandering, all contributing to varying reproductive strategies and outcomes.
At an opposite extreme, the bull elephant seal appears to have caught the female in a not too tender trap as a result of male resource guarding. Because seals often breed in low temperature climates, the females have evolved to have a counter-cyclical pregnancy and lactating season and gather on sheltered warmer beaches where they can nurse the pups often without feeding, using their blubber alone to keep both mother and offspring alive, at the same time becoming pregnant for the next season. A dominant male secures these spots before the females arrive and thus can guard a large harem (Low R427 44). The much greater size of the male is a reflection of the harem size and male competition. How efficient this counter-cyclical nursing has evolved to become is shown by the hooded seal who gives birth on ice flows and whose creamy milk with 60% fat can cause a pup to gain fifty pounds in a matter of days (Hrdy R330 129).
Sexual dimorphism: Elephant seals (Maier R431).
We should note that this form of male domination only exists because of the relative success of the female strategy of counter-cyclical pregnancy and breast-feeding. Females do secure superior genes for their pups, but at the cost of having some trampled by the bull and having to endure being raped and bitten by sub-dominant males should they leave the colony to fish (Low R427 45). A dominant male elephant seal can sire up to 90 pups and a female 10. Complementing the male strategy, it has been proposed that elephant seal females signal their receptivity to a broad array of males specifically to incite competition among the bulls to apply female choice genetically (Cox and LeBoeuf R135). Females apparently take advantage of this situation to actively pursue smaller subdominant males on the side, partly because they run a small risk (1/1000) of being suffocated by a large dominant male. Female choice between herding and time on the side is acting to keep the hugely larger male size in equilibrium (Sparks R654 13). In some seal species such as Weddell seal, dominant males may die from exhaustion at the end of a season. In others thy are simply overtaken exhausted by younger fitter males. On the other hand when a female seal leaves the colony she is liable to assault and rape by sub-dominant males who bite her if she doesn't submit. In some senses these patterns are not too different from human male dominant warrior societies trading their women as reproductive tokens where a Yanomamo village head such as 'Shinbone' sired 43 children by 11 wives (Chagnon R111 150). Much larger sirings have been made by human potentates who have clearly established the largest harems of any species. One in 200 people today carry the Y-chromosome of Ghengis Khan. One can only speculate where this would take human dimorphism, continued over evolutionary time scales.
An Antarctic fur seal trying to have sex with a king penguin. The brazenness of the seal's behaviour left those who saw it in no doubt as to what was happening (BBC 2 May 2008 http://news.bbc.co.uk/2/hi/science/nature/7379554.stm).
Sexual coercion among animals is extremely common: males of many species often harass, coerce or force females of their own kind to mate, while animals are also known occasionally to harass sexually a member of a closely related species. Harassment is common among pinnipeds, the group of animals that includes seals, fur seals, and sea lions; and occasionally it happens between related species. Male grey seals have been known to harass and mate with female harbour seals, for example, producing hybrids. Sexual harassment is often more commonplace in non-monogamous mating systems, and in species where males are physically much larger than the other sex and thus physically capable of coercion or harassment. But this is thought to be the first recorded example of a mammal trying to have sex with a member of another class of vertebrate, such as a bird, fish, reptile, or amphibian.Chinstrap penguins occasionally indulge in homosexual behaviour, and adelie penguins sometimes "prostitute" themselves to get stones for nest-building; while one in seven emperor penguins will change partners from one year to the next.
Orangutans have pronounced dimorphic male phenotypes. Degrees of phenotypic dimorphism may be very important in maintaining diverse mating strategies which enable a species to adapt rapidly to changing circumstances with now socialization patterns by altering the frequencies of the corresponding alleles in the population. Female coho salmon display a similar form of two phase female choice, in which there are two dimorphic forms of male, hooknoses which are fighting fit but took two seasons to mature and younger leaner jacks which came up river the first year. Contrary to expectations, females prefer the jacks, possibly because they are showing early fitness. Jacks just wiggle to signal an invitation and the females comply. By contrast they face a conflict of interest with the aggressive hooknoses who will bite them if they don't have sex (Mason R448). Roughgarden (R593) suggests that in polyphenic fish species there is reproductive cooperation between dominant male 'controllers', and the sub-dominant male phenotype which he calls 'cooperators', however the viability of this idea remains to be established. It is also doubtful that 'sneaker' male crickets, which sit silently behind a singing alpha male, assist the alpha, rather than exploit his efforts. Male cuttlefish are even known to become transvestites, assuming the form and colouring of a female to trick a dominant male and the female he is guarding into allowing his sperm to intervene in about a third of fertilizations (R288).
Male orangutans are called 'polyphenic' because there are two distinct male phenotypes, one a gangling 'peter pan' who tries to insidiously sidle up to and rape females, even when they are out of estrus, and the other an alpha male who beats his chest and roars through the forest enticing estrus females to his call (Hrdy R330 74).
The difference in reproductive investment strategies between the sexes, with males investing less causes the vast majority of animals to be polygynous. This applies consistently to invertebrates, fish and mammals. Only birds which uniquely are both egg-laying and warm-blooded are commonly monogamous because hatching the egg requires the cooperation of both partners. But even then, monogamy is social, rather than genetic and there are frequent clandestine affairs. Monogamy in the biological sense is social mating and does not imply sexual fidelity. Only 10% of 180 socially monogamous bird species are sexually faithful. Both monogamous birds and mammals clandestinely 'outsire' up to 20% of the offspring due to individual reproductive choice by either or both sexes to spread or extend their genetic investment.
Only about 3% of mammals are socially monogamous and only two monkeys, the marmoset and the tamarin, are truly monogamous. In mammals, where females both gestate live young and lactate, mating patterns are primarily determined by the way females distribute themselves, e.g. in relation to the food resource. Males will responsively distribute themselves in such a way as to guard either scarce resources (e.g. special territory) to monopolize females using them, or groups of females themselves (mate guarding) if they are wandering freely, foraging in wide areas in groups. At an extreme, if there are no means to monopolize female fertility, a few mammal species also resort to the lekking well known in birds, where males competitively display to the females for sex on an arbitrarily chosen stomping ground. Variations in how spread apart the females are in relation to plant food distributions in apes are believed to determine the spread from monogamy in gibbons through fission-fusion promiscuity in chimps to harem building in gorillas. Although the advantages of paternal help with child-rearing as well as widely spread females have been cited as factors predisposing to mammalian monogamy, the key factor appears to be simply how females use space (Komers and Brotherton R386). In many of the monogamous mammal species monogamy results not from male parental investment, but from males being forced to guard a lone female with a small exclusive range. In monogamous marmosets and tamarins, for example, females compete to pair with quality males and drive off competing females (Miller R475 185).
Prairie voles have become renowned for their pair-bonding based on the neuropeptides oxytocin and vasopressin (p 353). But their monogamy is unusual in that the founding pair are the sole breeders in a wider family group whose other females remain sexually immature and help to rear the young until they eventually mate with and form a pair bond with another outside male, causing the onset of ovulation and a new dynasty. Monogamous hibernating marmot mothers similarly engage aggressive displays towards their daughters as winter sets in causing them to fail to ovulate and remain with the nest, adding enough warmth to tide the next round of her infants through the cold spell. Noting its correspondence to human history Hrdy (R329 173) calls one female forestalling reproduction in another "the Hagar phenomenon". The coincidence of social monogamy and allo-parenting 'day care' is a common feature of mammal species in which the mother is adapted to produce a greater load in offspring than she can care for on her own. Cotton-top tamarins likewise depend on cooperative child rearing and give multiple birth to enable rapid population increase when the conditions are right. Mothers routinely give birth to twins and rely on the father or other group members to help rear them, or the babies may be abandoned within 72 hours of birth (Hrdy R330 180). In humans even one slow growing relatively helpless infant is more than a mother can easily care for and gather food for at the same time, so both pair-bonding and allo-parenting are readily evoked in a manner exceptional for other apes. The titi monkey is also monogamous. A couple regularly sit together on a branch, tails entwined. The mother is so engrossed with the father that she appears to pay marginal attention to her offspring, who drink from the mother, but cling to the father when she pushes them off. Nevertheless extra-pair couplings were observed in titis before female philandering in monogamous birds caused a sensation. Her attention to her partner makes perfect sense, because if he strays his resourcing commitment may be lost. As with tamarins and marmosets the female drives away females who enter her territory to avoid dividing her partner's attentions (R330 213). Infidelity in monogamy applies even to prairie voles: "What we say about prairie voles is that they'll sleep with anyone but they'll only sit by their partners" (Blum R66 95). It's no surprise that as soon as a prairie vole mates, he becomes more suspicious and aggressive of other males (R66 241).
Evolution towards extremely rapid increase in complexity, as exemplified by human cultural emergence, is consistent with a state of paradox in which neither sex is fully dominant over the sexual choices of the other, rather than any state of sexual dominion where the strategy of only one sex is brought fully into play. The emergence of culture is an abrupt process consistent with powerful sexual selection. The state of sexual paradox entices each sex to strive to gain the choice of the other through genuine indicators of fitness, involving both prowess and social astuteness as well as kindness and generosity to one's partners. These are all features characteristic of human emergence.
Moreover infidelity in modern society is something that is electively handled in relation to the stages of life's commitment, for example to raising children, and is not in any form a simple question of betrayal. In 2006 a study by of the British Sexual Fantasy Research Project led by Brett Kahr, found that the proportion of those having an affair increases with age group. 14% of under 30s in a long-term relationship admit to having an affair, 23% of 30s to 40s and 30% of over 50s. The average number of women a man has had sexual contact with is 15.64 and the average number of men a woman has had contact with is nearly as high at 14.56, scarcely consistent with our naive ideas of moral monogamy.
Key and Aiello (R359) have applied the prisoners dilemma game in detail to sexual relations in human emergence and concluded that "when male reproductive costs are less than female reproductive costs, males cooperate with females even when females do not reciprocate" entitling this 'non-reciprocal altruism' - an investment in a female and her offspring. The game showed that as costs increase, females will begin to help one another . Key notes: "That's because females have the same interests, such as food and child care". While it was to females' advantage to put all their effort into raising a small number of offspring, the best strategy for males was to attempt to father as many offspring as possible and not stick around to watch them grow up. However the model showed that males and females will cooperate when two conditions are met: first, when female reproductive costs are much higher than those of males, and second, if females can somehow punish uncooperative males. This associates with human emergence and the increasing head size of a larger and more complicated brain, motifs in which human females may have cooperated and applied forms of sexual enticement or even cooperative coercion to ensure male cooperation, possibly phased with the lunar and menstrual cycle (p 77). Noting that females are frequently more sexually active in socially monogamous species Enquist and Rodriguez-Girones (R195) developed a game-theoretic model to establish the idea that male 'fidelity' is driven by female 'deceit' in the form of concealed ovulation and opportunistic extra-pair couplings because the advantages to male philandering are reduced.
Parental Investment and Mother-Child Conflicts of Interest
Sarah Hrdy (R330 42) points out that selection of mothering traits is central to the equation of sexual evolution, particularly in mammals. "Over the course of her life, a female bound for fitness is required to make a series of physiological and developmental 'decisions' about how big to grow, when to mature, how soon to reproduce, and how much time to allow between offspring. One of the biggest challenges for understanding selection pressures on mother that confronted sociobiologists in the early years was getting the balance right between considering traits that are sexually-selected (for example through female choice or male choice) and equally important, if not more important, female traits that are naturally selected because they increased survival of the mother and her offspring." Females are thus applying a variety of skills in raising and caring for their offspring, all of which are critical and subject to natural selection for successful mothers in addition to sexual selection. In considering the question of reproductive sexual paradox we have to understand it not just in terms of sexual selection, but in terms of the overall reproductive strategies of each sex and their combined mating and parental investments. Sexual paradox is not thus a paradox of sexual selection but complete reproductive investment.
Although the female, particularly in gestating, lactating mammals invests more directly in parenting, the male's overall reproductive success is measured in offspring survival as well. Although a male elephant seal is primarily making a mating investment, his actions are part of a successful reproductive strategy in which his efforts are also indirectly parental. By providing a large harem with a warm relatively safe nursing space and driving off potentially infanticidal male competitors, and even ironically by killing off other males' competing offspring, he is furthering survival of his own progeny and hence his genes.
In "Mother Nature" Sarah Hrdy (R330) sets out a monumental account of why maternal ambivalence is a central evolutionary feature of the human condition with a long set of parallels shared in various forms by diverse primates and mammals. Many of these relate closely to the predominantly parental reproductive investment a female mammal makes and the trade-offs involved in dealing with limited resources, insufficient reserves, infanticidal males and the lack of condition and experience of a first time mother. In addition to the conditional mothering we have seen in the monogamous species such as tamarins and titi monkeys, she documents a variety of cases of maternal discretion, from absorbtion of a pregnancy in many rodents when an alien male makes an incursion which signals the threat of infanticide (R330 89), to maternal infanticide. In the monogamous California mouse a mother who loses her partner may kill the pups rather than try to rear them alone. This species is reputedly also monogamously faithful reflecting the fact that a bonded pair can raise four times as many offspring as a lone mother. Likewise to abandonment or even participatory cannibalism occurs in about one in ten prairie dogs when a pregnancy results in a newborn for whom the mother has insufficient resources (R330 93). Weddell seals likewise often abandon their first set of pups because they have not accumulated enough fat to support them through the nursing season, where they have little opportunity to feed.
Hrdy exposes a litany of forms of frequently resource-based maternal ambivalence in human practices of exposure, infanticide, and very large scale abandonment in European societies during the Christian era, which run completely counter to our idealistic notions of maternal devotion to the ultimate blessing of helpless dependent lovable yet demanding infants. Hrdy (R330 345) suggests that fixed strategies in other mammals such as reabsorbing a litter in mice and the biasing of sex ratios, for example in wasps are transferred to a discriminating maternal ambivalency in humans which leaves a decision whether to keep an offspring of a given sex to the last feasible moment, allowing for greater responsiveness to ecological and social contingencies. The consistent theme of this work is that, despite two conflicting views one of 'essentialist maternal instinct' and the other a cultural 'blank slate', human mothering responses are contingent, varied and a natural consequence of Hamilton's rule. "The cost function of Hamilton's rule calls [mother-infant harmony] into question. Instead of viewing it as an abnormality, a pathology to be treated , sociobiologists accept some degree of maternal ambivalence as inevitable. ... For as designed by Mother Nature, the delectability of infants seduces to quite different ends [from consuming them] ... to be consumed by them, to give up bodily resources, and time ... so that we could all (more or less) take our place at posterity's table" (R330 539).
In 1972 Robert Trivers (R703) extended Hamilton's rule of kin altruism to child-parent conflict. A child naturally shares all their own genes but only a quarter to a half those of their maternal siblings, depending on whether they have a common father. A child will thus settle for shared resources or attention only if it benefits a full sibling twice as much as the cost to themselves. Hence the apparent selfish greed of the squalling toddler vying for the attention of the mother makes genetic sense (Hrdy R330 427). It also applies to discriminating maternal responses to keep or abandon an infant based on its condition and potential impact on the viability of older offspring (R330 365), something Western society, still under the influence of patriarchal religions and social mind set, has great difficulty coming to terms with. In mammals, Haig's work shows the demands of the child in everything from placental invasion to relative size are partly a function of paternal influences.
Humans with massive pregnancies, difficult births and long periods of lactation and immediate infant care take an excessive toll on the mother. Hrdy (R330 175) expresses this succinctly as "a tooth for a child." Thus the prisoner's dilemma between mother and child is a direct extension of the sexual tug of war between sexually antagonistic paternal and maternal influences. One can cast this dilemma more generally in terms of parent-child conflict, but in most mammals the male reproductive investment is primarily in mating, rather than parenting and even in strongly pair-bonding humans the mother's child-care investment is primary. In the case of the male we, move from ambivalence to discriminating infanticide. In a large number of mammal species, males will immediately kill any offspring of a female they gain access to as a potential mate. Langurs are cautious and kill only infants which couldn't be theirs, both removing genetic competition and triggering early ovulation and pregnancy of their own offspring (R330 34). Chimps are less conservative and kill infants who might not be sired by the troop. Male mice have a biological clock which is primed to inhibit infanticide just long enough for a female they have impregnated to come to full term (R330 89).
It is the mother-child relationship and its implications for female autonomy that became the deepest evolutionary affront to feminist sensibilities. On the one hand we have a traditional patriarchal view, exacerbated by 19th century social Darwinism, of woman as merely a 'reproductive human' destined to be a mother rather than an innovator and expected to possess an unqualified maternal 'instinct' in response to the profound needs for love and security in the human infant, the absence of which is assumed to be a pathological condition. On the other we have a cultural view shared by many feminists, and a generation of anthropologists and sociologists that maternal reactions are culturally determined and that infants have no specific attachment needs but only desires.
Simone de Beauvoir pivotally expressed the concern that biological stereotypes would lead to the "enslavement of the female to the species and the limitations of her various powers". Reacting to attachment theory - the idea that human infants have an innate need for a primary attachment figure in the first years of life - a role that mothers are uniquely qualified to fill caused feminists to define female biological roles as 'essentialist' and to deny that biology is relevant to human affairs or that infants have innate needs for any personalized care on the basis that the human brain and our capacity for culture make us so different from other animals that humans can learn to be anything they choose.
Hrdy (R330 24) however notes that, although humans can learn a lot, this does not apply without biological restraint to such ancient emotional domains as those involved with 'love'. Nevertheless, the idea took on that maternal love was a socially-constructed sentiment without any biological basis." ( R330 308):
"Decades before the sudden-infant-death-syndrome scandals surfaced in the 1990s, or before data on foundling homes started to be quantified in the 1970s, psychiatrists, historians, and social scientists all noted the poor match between real-life mothers and nineteenth and early twentieth century stererotypes of instinctively nurturing mothers. Feminists in particular had long ago lost patience with Darwinian perspectives that struck them as essentialist and which patently disregarded womens felt experience. They were eager to discount biological explanations, and had little incentive to keep up with what was going on in reproductive ecology or sociobiology. They continued to project on to those fields their own worst assessments about essentialist and determinist assessments of 'female nature' even after biologists had themselves abandoned these types of explanations. The result was that feminist theorists were producing models to explain what was essentially a biological phenomenon (namely the failure of an infant to elicit nuturing responses from its mother) but without any reference to biology. They used the evidence of the high numbers of non-nurturing mothers as a tool to jettison altogether the confining stereotype of the instinctively nurturing mother that had long been used to prescribe social roles for women ... Instead of taking a closer, critical look at the original biologically-based explanations to see if perhaps something had been left out, feminists (along with other social scientists who were trying to explain the widespread practice of abandonment by mothers) patently rejected evolutionary explanations. The biological basis of motherhood was replaced by a new environmentalism. The way a mother feels toward her infant must be solely determined by her cultural milieu. - epitomized by Elizabeth Badinter's comment 'I am not questioning maternal love - I am questioning maternal instinct'."
This is echoed archetypally in Gerda Lerner's (R407 52) reaction to Freud's statement that for women "anatomy is destiny". "What Freud should have said is that anatomy once was destiny. This statement is accurate and historical. What once was, no longer is so, nor should it be so." Yet this biological destiny remains true for both men and women, so long as we reproduce naturally on the planet. Hrdy continues:
"Growing numbers of women were coming to regard attachment theory, [the idea that a growing infant had strong needs for a close mother] as an anathema. Rarely mentioned in feminist circles, [John] Bowlby's name, when it did come up, was uttered with derision. Why might women have a stake in discrediting research ostensibly focussed on infant well-being? Having panicked often enough myself over whether I could live up to the stiff responsibilities of motherhood I understand why" (R330 489).
Just how sensitive this issue became is etched out by Hrdy (R330 406):
"Compared with Darwin's 'dangerous idea' the evolutionary philosophy that Daniel Dennett has termed 'universal acid' because it cuts so deeply into human conceits about our place in the universe, Bowlby's intellectual acid was less corrosive. Yet for psychoanalysts, for feminists and for any woman with ambitions, it burns very deeply indeed. ... By situating the mother (or primary care taker) at the center of each developing infant's universe, Bowlby's theory of attachment stings most smartly where it pricks the conscience of every mother who is aware of her infant's needs but who aspires to a life beyond bondage to them".
Hrdy notes that the debate over whether or not women have 'maternal instincts' has taken decades to unravel to the point where the patriarchal assumptions of earlier generations of moralists have been corrected and 'Darwin's evolutionary paradigm widened to both sexes. But by this time, feminists, social historians and philosophers were convinced that what evolutionists had to offer was essentially flawed, determinist and uninsightful. Natural selection, and with it the most powerful and comprehensive theory available for understanding the basic natures of mothers and infants was rejected, as feminists and social scientists took a path, rejecting biology and science, constructing their own version of wishful thinking about socially constructed men and women, and infants born with merely a 'desire' for mothers rather than a 'need'. Maternal love could then safely be interpreted as a 'gift' consciously bestowed, or a by-product of changing fashions and sentiments. The more multifaceted view of mothers, being developed by biologists, featuring flexible actors whose responses were contingent on circumstances went largely unheeded. "Lost in the shuffle over what it was natural for mother to do and dust ups over bonding and mother love was the infant's often noisy two cents worth "No matter who gives it, I need it. And need it now."
Hrdy (R330 535) notes that Bowlby provided scientific legitimacy to the anxiety, distress terror and finally desolation that infants experience when they fail to detect 'the meeting eyes of love' and that although many of the dangers turn out to be different from those he initially envisioned, his central explanation of how and why infants become attached to their caretakers was on target. He was correct that primate infants, including humans, are born immobile and vulnerable. He rightly pointed out that they respond very poorly to being left alone, or otherwise being made to feel insecure. Human infants have a nearly insatiable desire to be held and to bask in the sense that they are loved. To this extent the needs of human infants are enormous and largely non-negotiable. The question that remains is, what are the implications of this for their mothers? Part of the problem is that there is little agreement about whose interests are to be maximized in a world where conflicting self-interests, are endemic between parents and offspring, between mothers and fathers, within families, between families. Hrdy comments:
"Understandably, perhaps, those most threatened by acknowledging infant needs - mothers with aspirations to do things other than mother - were the ones who felt most compelled to down play infant needs" (R330 493).
We see in this a succinct expression of Hamilton's rule and the extension of sexually antagonistic coevolution striking home directly to the feminist reaction to the mother-child issue in a strategic attempt by mothers, if not to entirely gain control over the infants their reproductive investment depends on, by a culturally relativistic finesse, at least to regain from moralizing males the freedom of choice for that very maternal ambivalence that lies at the root of the Prisoners' Dilemma of long-term survival between mother and offspring.
This discussion of the mother-child relationship raises a further question about the role of the father. Hrdy has proposed that much of the child-rearing effort in early humans was done by allo-mothers or allo-parents - other helpers, such as older daughters, sisters, relatives such as aunts and uncles and reciprocal female friends in addition to or in spite of the father's role, which in most societies does not come anywhere to a near match to the mother's at least in the early years. This follows a mammalian pattern in which mothers who need extra help do so from several sources even in many socially monogamous species. It is notable that in Sandays' (R609) survey of human societies that in most societies fathers were involved only rarely or occasionally with child care.
This leads to another interesting hypothesis. Judith Rich Harris (R292, R293) has all but demolished the socialization theory of parental molding as a process of reward and punishment, however the genetic links between the personalities and many aspects of the mental life of parents and children do have a manifest genetic basis. Her alternative hypothesis - that the peer group forms the major influence on the socialization of the growing child also has a basis in evolutionary sociobiology. As Ridley (R580 259) points out the peer group provides a context for niche diversification and specialization of a growing individual to find skills and specialities a growing person discovers are appreciated and sought after by the group they will spend their early adult life with. The formative influences on children during human emergence are likely to have been a fluid mix of influences from their mother, father, allo-parents, extended family and peer/play group in a small band of gatherer-hunters, rather than a rigid nuclear family structure. We are thus likely to see young humans genetically kin with their parents sharing a vertical affinity across the generations while engaged in a struggle of partial conflict of interest. At the same time they have an adaptive horizontal social orientation towards the peer groups which will also be essential in their social survival.
The major theme of Ridley's (R580) "Nature via Nurture" is that the biological role is not one of genetic determinism, but of genes adaptively