Why Did Sex Evolve?
Some reproduction is sexual and some is asexual. There is no biological necessity about sexual reproduction, despite its prevalence. How could there be any such necessity, given that the basic principle of evolutionary biology is just that organisms are designed to maximize the presence of their genes in later generations? This says nothing about mixing genes or about a division between the sexes. Why not reproduce purely by cloning? Why isn’t all genesis parthenogenesis? This seems perfectly possible, much simpler, and evidently how reproduction began on planet earth. So why did sex evolve from non-sex?
The problem is not just that no obvious adaptive rationale for sex seems to suggest itself; there are positive reasons why the existence of sex seems to violate basic principles of evolutionary biology. The most obvious point is what might be called “gene dilution”: instead of passing down a hundred percent of one’s genes, one passes down only fifty percent. In parthenogenesis a hundred percent are inherited, so surely an organism would prefer that figure to a mere fifty per cent. Genes that build bodies that pass on only a fraction of themselves will not be as frequent in later populations as genes that pass on a hundred per cent of themselves. Sexual reproduction appears to thwart the prime directive governing genes: maximization. Second, in sexual reproduction it is necessary to find a suitable sexual partner, whereas in cloning you can go it alone. That requires expenditure of energy and risk of failure: why take such a hard road when parthenogenesis enables one to stay home alone and get on with the job without going out in search of unreliable mates? Third, from the female’s point of view sexual reproduction looks a lot like altruism: she is providing a service to the male by passing on his genes, using her own energy resources, for which she does not seem adequately recompensed. She seems to be doing the male a favor, but organisms built by selfish genes don’t do each other favors. The role of female looks unacceptably altruistic. We need to show what is in it for her genetic prospects. Why tolerate males at all? Why aren’t all organisms female?
Sex thus appears biologically paradoxical—inconsistent with even the most basic principles of evolution. We must find a way to explain its origin and persistence that comports with basic biology. Many theories have been proposed, which I won’t discuss here. I intend to propose, as economically as possible, another theory, which respects the game-theoretic selfish gene perspective now prevalent in the field. I call this the “genetic parasite theory”.
Imagine a population of single-celled eukaryotic organisms (ones with a sheathed nucleus containing DNA) and suppose their mode of reproduction to be asexual. They are all, in effect, female, and reproduce by cell division, transmitting one hundred percent of their genes into each offspring. Now, life being what it is, opportunities for parasitism will arise: some of these cells may adapt to exploit the resources of other cells in the population, without killing them. Let us suppose that they attach themselves to the surface of host cells and siphon off nutrition found in the host. The host will resist such nutritional theft, but it may persist nevertheless, possibly following an arms race between parasite and host. Being a parasite is always a highly attractive option for any evolved creature, having all the benefits of theft over honest toil, and is not easily foiled (it is really just a kind of non-fatal predation). But suppose that some cells are more ambitious: they seek not just food but also reproductive assistance—they want to use other cells to pass on their genes, sparing themselves the expense and trouble. They therefore evolve a pointy organ that can penetrate the surface membrane of other cells and transfer their own DNA into the nucleus of the host cell, where it can enjoy the resources of the host cell in getting itself reproduced. These cells are not nutritional parasites but genetic parasites. They might even be able to replace entirely the DNA of the host cell, by inserting all their own DNA into the nucleus. That would mean that none of the host’s genes are transmitted and all of theirs are. By the laws of gene selection such a host would soon go extinct; its offspring would be copies of the parasitic cell. We would thus expect that counter-measures to the genetic infiltration would evolve, and an arms race would develop. The host cell might develop ways of poisoning the parasite or dissolving its genetic residue once inside or blunting its pointy organ. Let us suppose that an equilibrium point is reached in which fifty percent of the parasite’s DNA is permitted inside the host’s nucleus and fifty percent of the host’s DNA remains. Perhaps if the host accepts this amount less damage is done to it by the invasive cell, which will limit its aggressive incursions if the host cooperates to some extent (otherwise it will fight to the death). Still, this is a highly unsatisfactory outcome for the host, because of gene dilution. How might it adapt to this state of affairs? It needs to find a way to get something out of the new arrangement—some sort of genetic payoff.
Some of the genetic parasites will contain better genes than others. If poor quality genes are mixed with the host’s genes, then the result will be less advantageous than if good quality genes are mixed. Given that the host is losing fifty percent of her genes in the new arrangement, it would clearly be better if she were to have good quality alien genes than poor quality ones, since the whole package will then do better, which is good for her genes. So she begins to favor parasitic genes that are better than others—she exercises quality control with respect to her genetic parasites. She becomes selective in her resistance. She is still not as well off genetically as she was before all this happened, when she reproduced by solitary cloning, since she is still suffering from gene dilution. But there is little she can do about it given the aggressive parasites she has to contend with. It is always better to have no parasites than some, but it can be better to have some parasites rather than others. You want the ones that can do you a favor in return, if that is at all feasible. Thus our host will want to select the best genes she can from her would-be parasites, because these will aid her own genes better than other parasitic genes will. The situation is still unstable, however, because there will be selective pressure to revert to the pre-parasite state of things, where all of her genes get perpetuated. She will want to resist the genetic parasites as much as possible, consistently with the arms race and the costs of resistance. How can things be made more palatable to her?
Suppose that among her “suitors” a select few have genes with the following property: if they are combined with hers they will actually increase the chances of her own genes surviving into the future, relative to their chances without such combination. Given genetic variation in the population, some cells will be more viable than others—and these are the best ones to “mate” with. In other words, the optimal strategy for an invaded host cell is to select a parasite that will improve her genetic prospects—not just relative to other potential parasites but also relative to her chances without such parasites. If she mates with such a fine specimen, then her genes will actually be better off than if she reproduced all on her own. True, there will be fewer of her genes in the next generation, but by combining with genes superior to her own she will ensure that more of her genes will eventually survive and reproduce. The result of this kind of upgrade combination is a “leg up” in terms of genetic survival, compared to the way things used to be. This, then, is how sexual reproduction evolved as a stable mode of reproduction: genetic parasitism combined with genetic selection that provides a “leg up”. What started as straight parasitism, with the usual arms race and compromise, turned into a kind of symbiosis, when the female improved her genes’ chances by selecting high quality “male” genes. Now there was something in it for her, beyond simply minimizing the bad effects of determined parasites. If she could have won the arms race against the parasites, reverting to her untroubled asexual mode of reproduction, that would have been quite satisfactory; but it is even better to find a way to exploit the parasite by selecting only parasites that serve her own genetic interests better than the old regime. And if she could not win the arms race anyway, it is better to turn a fait accompli into an unexpected triumph: the female cells that are better at selecting the male genetic parasites with the best genes will do better than those that are not so good at this. Thus we get competition among males to be selected and competition among females for the best males.
Here are a couple of analogies to bring out the logic of the situation. Suppose there was a parasitic worm that could actually affect the DNA of its host: it secretes a chemical into the DNA and changes its composition, producing new genes. Suppose some of these worms produced worse DNA and some produced better DNA. Clearly it is to the advantage of the host organism that it selects the worms that improve its DNA, since these will then have a better chance of being passed on. It might be better to have no such worm, but given that this is unavoidable, natural selection will favor the “good” worms over the “bad”. And maybe there are some worms so good that it is better to have them than to have no worms at all—since they can build organisms greatly superior to any built by the host’s original genetic composition. These super-worms produce simply outstanding children for the host. Similarly, alien DNA (deriving from a “male”) might so improve the female’s gene complex that the necessary genetic dilution is acceptable, according to the genetic calculations. Fifty per cent of my genes surviving for a thousand generations is a lot better than one hundred percept surviving for only ten generations. It is like five of my ten children living to be a hundred with the other five dying in childbirth, compared to all of them living only to the age of three. A worm that re-tooled your genes to make them substantially better at surviving would pay its way in the unforgiving genetic arithmetic. Genes for tolerating such a worm would be more likely to be passed on.
The second analogy concerns coalitions. If someone comes to you to form a coalition in order to secure some future benefit, you must ask yourself a simple question: am I better of with her or without her? If I can secure the benefit without the coalition, I do well to decline her offer, since I would then have to share the benefit. But if I judge that I cannot achieve the end without her help, then I should join with her in a coalition, since I will get nothing otherwise. Sexual reproduction has the same logic: if my genes go it alone they have a certain probability of surviving to reproductive age (maybe zero), but if I combine them with someone else’s genes (losing fifty per cent of them, say), then there is a different probability of their survival. If the latter exceeds the former, then I am rational to choose the latter over the former. A potential mate is like someone offering you a coalition: if you mate with me I assure you the chances of genetic happiness are high, compared to the chances if you mate with someone else or just decide to go it alone. Suppose you happen to have both means of reproduction available to you, sexual and asexual. You have to choose which to employ. You compute the payoffs by multiplying the number of your genes that will get passed on by the probability of their survival (over, say, the next million years). If a hundred per cent get passed on by the asexual method, but there is a low probability of their long term survival, you might opt for the sexual method where fewer get passed on but the probability of survival is much higher—but only if you believe the “donor” genes have this kind of survival power. In the same way, your coalition mate has to be good enough to warrant dividing the spoils with her later, or else you will choose to go it alone and keep all the spoils for yourself. Sex arises from genetic coalitions, possibly preceded by genetic parasitism. This is better for both parties, because there is something in it for the host and the parasite benefits because its incursions are no longer resisted. Thus we move from resistance to consent: the male benefits but so does the female. This solves the problem we started out with, which was to explain how sexual reproduction could make sense given that asexual reproduction seems so much more sensible biologically. The answer is that it results from a strategy for dealing with genetic parasitism.
Let me restate the point in less abstract terms. Why should a female mammal allow her womb to be colonized by a male mammal with a different set of DNA? Why should her energy resources be diverted into generating his child? He should take care of it himself! He is just freeloading off her womb and energy resources. The suggested answer is that she is gambling that the influx of his genes will improve the prospects of her genes. Given that the male would just parasitize her womb anyway, it is better to be selective about mates and try to improve her own chances in the genetic lottery. In the payoff matrix that describes all the options, with their various costs and benefits, sexual reproduction seems the best choice—the best compromise, we might say. Asexual reproduction makes perfect biological sense—it is how a well-meaning Creator might have arranged things—but given the rough and tumble of evolution, with the ever-present threat of unscrupulous parasites, sex has emerged as a kind of game-theoretic solution to an inevitable problem: namely, what to do about those pesky genetic parasites. The parasites are with us always, given the attraction of that line of work; the question is what can be done about them. And the answer in one word is: compromise. Sex is a kind of accommodation to the harsh reality of biological existence—ultimately, access to energy.
If this explanation is on the right lines, what might we expect to characterize animals and their sexual behavior? One point has already been mentioned: we would expect male competition for females, selectivity from females, and competition within females for outstanding males. Of course, these are all abundant features of animal behavior. Correspondingly, we would expect female sexual anatomy to conform to the general theoretical picture: it should not be too easy to impregnate the female, which would impair her ability to be selective. Her consent to copulation should be required for copulation to be feasible for the male. Rape should be, at least, difficult and potentially hazardous. At the same time, copulation should not be so difficult that a suitable male is just not up to the task: hence difficult but not too difficult. We might also expect sex to be somewhat predatory, given that the male is always essentially exploiting the female, in order to spare himself the effort of gestating offspring; and the female will always be wary and choosy, wondering if this suitor is really “the one”. She is giving up a lot to incubate his progeny, in terms of energy and commitment; so she has to be sure there is something in it for her (i.e. her genes). The genes of the female must move her in such a way that their interests are respected, even though only fifty per cent of them will end up in the next generation. The genes of the male have no such concerns, given that he is not called upon to act as incubator; and he can spread those genes around ad libitum. The underlying logic of sex predicts these kinds of phenotypic facts, and they are evident enough in animal behavior. Fundamentally, the male is still the aggressive parasite and the female the reluctant host trying to make the best of a bad job. Of course, once the sexual machinery is in place and the female has no other reproductive option, she will act with enthusiasm and commitment; but the genesis of sexual reproduction is still written into the underlying structure of the sexual relationship.
A less obvious consequence concerns sexual selection. The female exercises quality control: she evaluates her potential mates by formulating hypotheses about their genetic fitness, based on what she can observe. She cannot peer directly into the suitor’s genes but must go by outward appearance. Thus she espies the peacock’s lavish tail and infers genetic superiority within. This causes males to improve their appearance so that females will evaluate them highly: but to improve their appearance they have to improve their reality. They have to be bigger and stronger, less infested with parasites, and more able to sustain pointless bits of flamboyance. So there is selective pressure on males to improve. Thus sex leads to sexual selection, which leads to improvement. That is, sex is what powers evolution to produce ever more complex and accomplished animals, via sexual selection. But asexual reproduction has no such consequence: the organism just reproduces itself according to its original design. There is no sexual selection when reproduction is asexual, and hence no motor to drive biological progress. The result is likely to be stasis, uniformity, and dullness. You don’t get complex beautiful animals when the method of reproduction is asexual. It is not, of course, that anyone is aiming for such complex beauty; it is just that the mechanism for producing it does not exist in a world without sexual reproduction. We owe it to sex to kick start evolution into a higher gear; before sex the pressures for change were minimal. It was when females started to be choosy, as a way of making the best out of living in a world of genetic parasites, that sexual selection triggered the kind of evolutionary changes that we see. Without sex Earth might never have got beyond boring bacteria floating in nondescript oceans. We owe it to the parasites among them to have initiated a process that led to the impressive variety of animal life that now exists.
Here is one final point–a kind of theorem: a genetically perfect female has no rationale for engaging in sex in a world in which she is subject to genetic parasitism. If she cannot improve her genetic fitness by merging her genes with those of a male, then she has no motive to permit her body to be used as incubator. For her, all genetic mixing is genetic degradation. She therefore has every reason to fight off all male incursions. But the same is not true of a genetically perfect male: he still has every reason to reproduce sexually, since he can thereby produce more copies of his genes than by solitary cloning. He just has to deposit them in as many willing (or unwilling) female bodies as possible. There is a huge logical asymmetry between being the one with the incubating body and being the one who uses someone else’s body as incubator. That asymmetry is the real basis of sexual reproduction (and indeed ultimately defines the difference between the sexes). Genetic perfection in the female leads naturally to frigidity, but genetic perfection in the male entails no diminution of sexual appetite. In other words, the genes see no point in sexual reproduction for the genetically perfect female, but they see a lot of point in it for the genetically perfect male. Of course, there is no such thing as genetic perfection in the real biological world–but I am making a purely logical point.