The biological analysis of sexual behavior in the context of evolution and natural selection

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As mentioned in the preceding section, there is a long tradition for teleological explanations in parts of biology and biological accounts of sexual behavior are no exception. The reproductive consequences of sexual acts are thus paramount in any analysis of sexual behavior as soon as a biologist is involved. It is tacitly or explicitly assumed that evolution has assured that sexual behavior is as efficient as possible for fertilization to occur.

An analysis of sex behavior in terms of biological function and evolution rests on some or all of the following assumptions:

1 The purpose of sexual behavior is fertilization. The purpose is also the cause.

2 Evolution has maximized the ability of sexual behavior to achieve fertilization.

3 If two or more different behavior patterns existed, then evolution has assured to eliminate the less efficient ones.

This means that all kinds of sexual behavior patterns not leading to fertilization should have been eliminated through the course of evolution. Furthermore, no one would engage in sexual activity if fertilization were not at least potentially possible. Non-fertile sex carries a cost to the individual but no benefit and any tendency to engage in such behavior should have been disadvantageous and eliminated through the process of natural selection. Finally, the behavior patterns expressed should be efficient for assuring the union of gametes with the least cost possible. That probably implies that copulation should be as short as feasible and the least physically exerting as feasible.

Let us briefly examine each of these suppositions. We have already discussed the problems with teleology quite extensively, so I will not do it again. The second and third assumptions are worthy of some analysis, though. If evolution had maximized the ability of sexual behavior to achieve fertilization, it should have assured that sex behavior only occurs when the individual is fertile. Any individual showing behavior outside of fertile periods should have been forced to carry extra costs and should have been extinguished. If we accept assumption 2, we must also accept that women represent one of evolution's failures. Females of some primate species in addition to Homo sapiens have also the privilege to share this position. Men are not better, in fact. They accept copulation with unfertile women, some even with insistence and pleasure. Males of many other species have the same bad habit of trying to copulate with unfertile females. A sexually experienced male rat may be just as insistent and persistent as any man when trying to copulate with an unwilling female. A female rat may be unwilling because she is prepubertal or because she is not in estrus. In both cases she is unfertile. I will not multiply the examples, but it is quite evident that evolution has failed to assure that sex behavior maximizes the possibility of fertilization. Having sex when not fertile is incompatible with the basic criteria of natural selection and sex with an unfertile individual is equally futile in an evolutionary perspective. We have at least three alternative solutions to get away with these imperfections. The first is to accept that natural selection is far from perfect and has allowed many inadaptive behaviors to persist. This, in turn, means that it is risky to assume that behavior is always adaptive. The second is an extension of the first, in the way that it is maintained that evolution has not shaped the intricacies of sexual behavior because natural selection has failed to exert systematic pressures on specific behavior patterns. The third is to invent elaborate and often quite esoteric arguments as to the adaptive advantages of showing inadaptive behavior. Personally, I favor the second alternative.

Considering the third assumption, the evidence in favor is mixed. Sometimes evolution seems to have been quite efficient. A rabbit, for example, shows a very efficient sexual behavior - one single intromission, always associated with ejaculation. It is all a question of about one second. Very efficient in time and in effort. Moreover, the doe is a reflex ovulator. She displays lordosis, making vaginal penetration possible, only when in estrus and when in estrus she is always fertile. Shortly after copulation, the female will ovulate and fertilization is almost certain since the male deposited semen a few hours earlier. After ovulation, the propensity to show lordosis will soon be reduced and finally absent. It would seem that evolution has done a good job, assuring that sex behavior in rabbits is fast, almost effortless, and frequently fertile. It is not so easy, though. A male rabbit may spend hours mounting an unfertile female if given the opportunity to do so. Although his sex behavior seems very efficient, it is not certain that it really is. It is not known how much time a wild male rabbit engages in mounting unfertile females, but it is not unlikely that it is far superior to the time he spends copulating with fertile females. If this indeed were the case, then his behavior would be quite inadaptive.

A male rat needs to make a large number of vaginal penetrations, intromissions, before ejaculating. The number varies often between 6 and 12, and the time investment can be from under a minute to up to half an hour or more. Since the female has the habit of running back and forth, and indeed has to run back and forth in order to incite the male to mount and intromit, it becomes a rather exhausting exercise. A poor rat needs to expend a lot of time and energy in order to deposit sperm. Extremely inefficient compared to a rabbit. Sexually experienced male rats also spend some time mounting infertile females, when given the opportunity, making their sex behavior still more inefficient. The inefficiency of the male rat's sex behavior is often explained as a consequence of the fact that the female rat requires several intromissions for successful implantation to occur (Adler, 1969) and that his behavior in fact is very adaptive. This is pure nonsense, for there is no a priori reason for the female rat to require many intromissions for subsequent successful implantation of the fertilized ova, thereby being far less efficient than a female rabbit.

There are innumerable examples of inefficient sexual behaviors among mammals and many of very efficient behaviors. The question is why the inefficient behaviors have not been eliminated through natural selection. They seem rather to have been rewarded. The rat is a real cosmopolitan. In fact, just as cosmopolitan as the human. Rabbits much less so. Many explanations have been advanced for the existence of dramatically inefficient sexual behaviors, all having in common that they try to invent adaptive advantages of clearly inadaptive behavior through long-winded and often surprisingly creative teleological arguments. Another explanation for the persistence of inefficient sex behavior is that there are so many characteristics and combinations of characteristics that determine the overall fitness of an individual that details of sexual behavior have a most limited impact. Natural selection operates, probably in a most efficient way, on all characteristics having significant influences on fitness, but far less so or not at all on characteristics having only marginal impact. This reasoning could explain the great variety of sexual behaviors that can be found in mammals, not to mention in other vertebrates. This variability stands in sharp contrast to the limited variability in other systems. The cardiovascular system, for example, is essentially identical in all mammals, both with regard to anatomy and physiology. The reason is probably that cardiovascular functioning is essential for survival and even small variations in the efficiency of this system are associated with substantial differences in fitness.

The preceding paragraphs should have illustrated that none of the basic assumptions in the traditional biological analysis of 'reproductive behavior' is supported by fact. They can be saved, though, by making still more assumptions about adaptive-ness, by giving a purpose to inadaptive behaviors. When these additional assumptions are challenged, then additional assumptions can be made in order to save the previous ones and so on in eternity. The most reasonable conclusion is that it is unknown how much selective pressure has been put on sexual behaviors. The margin for random variation is, consequently, unknown. My guess is that evolution, through natural selection, has been quite generous in allowing sexual behavior to be quite inefficient and highly variable between one species and another. A wide margin of random variation, unavailable for natural selection, implies that speculations about evolutionary advantages are basically meaningless. Away to make sense of a senseless (random) world.

I have many times mentioned that biology likes to offer teleological explanations of sex behavior and, consequently, that the purpose and cause must be reproduction. I have also analyzed how a Darwinian analysis of sex behavior suggests that the only adaptive sex is that associated with reproduction. Teleology and evolutionary theory have merged in the conclusion that sex must be associated with reproduction and, if it is not, it is inadaptive. The next step is to say that inadaptive sex is antinatural. This kind of reasoning has, in some societies and at some points in time, led to the tragic notion that humans displaying non-reproductive sexual behaviors are inferior to those that display sexual behaviors that potentially can be reproductive. Among the many behaviors considered anti-natural or inadaptive are sexual activities with individuals of the same sex, cunnilingus, fellatio or anal sex. All these activities were and still are, at some places, not only regarded as inferior but also severely punished either by social opprobrium, penal action or both. Biologists have provided a scientific rationale for such actions through their use of evolutionary theory.

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