A Discussion on Sexual Selection
I. Introduction
In human social interactions, there is a general pattern for sexual selection in reproductive success � that is, an attractive or powerful individual will be more likely to be selected for than the average person in our short-term human evolution. Darwin was first to apply this notion of reproductive struggle to the behavior of animals, in his 1871 tome The Descent of Man and Selection in Relation to Sex. He writes that:
Males have acquired their present structure.. not from having better fitted to survive in the struggle for existence, but from having gained an advantage over other males [in reproductive access to females], and from having transmitted this advantage to their male offspring�it was the importance of this distinction which led me to designate this form of selection as Sexual Selection (Darwin 569).
The distinction from natural selection is apparent when one sees that the secondary sexual characteristics that tend to increase reproductive success are not necessary. At times, they can even be detrimental to the function of the primary sexual characteristics that are directly involved with reproduction. The long train of the great bird of paradise is a prime example: it is fairly inhibitory to survival, but it is quite important in its reproductive success among female birds of paradise (Figure 1). Initially, Darwin received little approval or interest from other evolutionary thinkers, notably Alfred Russel Wallace and Theodosius Dobzhansky (Wallace, Dobzhanksy). The general scientific community tended to disregard sexual selection because individual variation was not very highly thought of, so long as reproduction continued. Others retained the peculiar Victorian notion of female disinterest in sex and thus utilized a moral criticism of Darwin�s postulates. However, the redoubtable logic of such a position began to ingratiate itself on the scientific mind, leading to the general theories of Zahavi and Fisher and the explosion in sexual selection studies through to the modern day.
II. Male Competition
Darwin posited that sexual selection would come in either of two forms. In one form, usually known as intrasexual selection or male competition, sexual selection would come about as a result of fighting with other males for the chance to mate with a female. He attributed the �useless� presence of horns and spangles to their use as weapons for advantage during these male competitions (Darwin). Even in the modern era, those sexual modifications involving better adapted combat traits are quite prevalent in nature and receive much attention from biologists. The implication is that the so-called winners should be more vigorous than his competitors, and thus future offspring should also be as vigorous. In a study of courtship among Drosophila, John Maynard Smith found that females tended to reject those males who could not complete the intricate mating dance (Maynard Smith 1956). These unfortunate few were usually the result of high mutational loads or poor adaptations to novel environments, all signaling poor survival traits. His results addressed two issues which had been weaknesses in Darwin�s original formulation: false advertising of genetic quality could skew selection, and there would be no selection if advantageous genes could be so quickly fixated (Bell). These female �tests� of competition would ensure that there could be no false advertising. Also, the assessment of mutational loads and adaptations by female behavior would allow for preferential mating without losing genetic variance, through the fluctuations of mutation-selection balance and frequency-dependent selection traits such as infection resistance.
Heritability, the proportion of differences in traits due to genetic differences, usually plays a large role in evolution through sexual selection. However, it is also possible for non-heritability to be a vital contribution during male competition. Amotz Zahavi�s handicap theory conceived that survivors of competition with some non-heritable handicap must have extraordinary survival and adaptation skills despite the obvious maladaptation (Zahavi 1975). He argues that these males thus have superior genes that can be passed on with higher selective advantage to their offspring, without the negative effect of inheriting the accidental handicap. The fact of this test�s costliness tends to promote its reliability as a measure of sexual advantage. This theory does encounter some difficulty with selection. Selection automatically reduces the inherent heritability of fitness in Zahavi�s theory and hence leads to fixation. This problem is adequately addressed by the fact that variance can be maintained by mutation-selection balance and frequency-dependent selection as mentioned above (Heino et al. 1997).
As a residual effect of sexual biases in human social institutions, it is mostly assumed that males are necessarily the more aggressive creature in the relationship, and females the more �coy� type. Though male dominance is present in most cases, there are significant examples of a reversal of these stereotypical roles through female competition in nature, especially among female-dominated systems. Bengt Hansson and colleagues observed the interaction of primary and secondary great reed warbler females and found that the eggs of the primary females were being targeted by the secondary females (Hansson et al. 1997). Warbler males allocate fatherly aid to the females in accordance with the appearance and continued existence of their clutch � thus, infanticide would destroy the primary female�s clutch and allow the male warbler�s attention to move on to someone new, increasing the chance that the secondary female would be next in line. Patty Gowaty found female eastern bluebirds to be murderously aggressive in claiming and delineating their territory (Gowaty 1997). Even more brutal are the social insects � the honeybees, the wasps, the hornets � whose entire social structure revolves around support for the queen. The queen supports her own survival by killing her competitors, while the workers ensure their own by planting their own eggs in the hive or manipulating brood numbers. Mary Jane West-Eberhard, when working with paper wasps, found that females worked better in groups, but the dominant wasp would be rewarded most in terms of reproduction (West-Eberhard 1979). This ensured a continuous and violent struggle for domination within the hive. These conclusions help to correct some of the masculine characterizations common in evolutionary research, but there are still significant traces of human bias and sociological generalizations that can prove misleading in a study of evolution.
III. Female Choice
The other form of sexual selection, epigamic selection or female choice, has been passionately debated since its debut on the scientific scene. Malte Andersson was able to show that the existence of long tails � natural or artificial � attracted more female attention than did normal tails in the case of the African widow-bird (Andersson 1982). In a study of peafowl, Marion Petrie discovered similar results using the manipulation in numbers of eyespots on their tail feathers (Petrie 2002). Interestingly enough, the offspring of the more successful birds were heavier and more likely to evade predators, both traits of higher survival. Female choice in these studies tended to be open ended rather than absolute; that is, the preference was only for more exaggerated characters rather than specific detailed qualities.
Darwin originally envisioned this female choice as a pre-existing bias that was generally unselective, or at most, could be explained by some other part of the creature�s evolution. However, Sir Ronald Fisher was able to come up with a more graceful explanation of the existence of female choice � the runaway sexual selection model (Fisher 1915, Genetical). He conjectured that female preference began with heritable traits that were already favored by natural selection. The ability to choose fit mates through these traits would end with fitter offspring and enhance discrimination for that trait by increased viability and sexual success. In the next generation, sexual selection would ensure both increased female discrimination and exaggeration of the male trait without any positive adaptation for the trait�s original function, leading to heightened conflict with natural selection. Only when natural selection pressures rose too high would sexual adaptations stop (Figure 2).
Critics of female choice tend to disagree with the mechanism by which female choice arises. They concede that preference for certain traits might exist, but this does not dictate how animals themselves view the trait. A study of cricket songs found that females indubitably chose the males with the �longest� and flashiest songs, even if they were merely recorded and played back (Hedrick 2000). In a study of cichlids, the female colored fish preferred males of the same color (known as positive assortative mating) unless the water was cloudy, in which case males of either color had no advantage (Seehausen and van Alphen 1998). In the first study, there is significant proof for some sort of artificial sexual selection, but it does not dictate an ingrained preference in the natural state. The second study shows the marketability of the color trait, but at the same time, it gives no reasons. Are familiar colors more adaptive to certain conditions? Are they more attractive? It isn�t quite clear what makes them selected for.
Other issues come up once one views human situations of female choice. For example, it is a general trend that the more attractive mate in a relationship can get away with doing nothing, while the less attractive individuals in the pool must compensate by showing that they can work harder with the offspring. This doesn�t mean that female choice in animals can possibly work the same way � for example, there are no similar decision-making components in animal brains, and even among humans, female choice often does not apply, especially in older cultures where marriages were more strictly controlled. Science does not know enough about the intricacies of animal culture to be able to refute the possibility of prohibited female choice in animals. However, evolutionary biologists only need to contend with proving the existence of sexual selection and in this case, of female choice. They need not be too concerned with the various thoughts running through the female mind before selecting a mate, only with the evolutionary outcome of her decision.
IV. Parental Investment and Genetic Survival
As biologists study evolutionary models, there is a tendency to humanize the animals used in each simulation of nature. However, selection in nature has less to do with the individual motivations for reproduction than with the passage of genes by maximizing reproductive success. It is the genes that are key, as they are the basic units of evolution. The question does arise: are genes inherently selfish? The answer should be a resounding yes, as the essence of reproduction is passing along one generation�s genetic heritage to the next. Within sexual selection, this makes for a more elegant, logical and neutral explanation for the existence of such anomalies as high promiscuity, differing clutch sizes and variations in parental investments.
Robert Trivers was first to propose the idea that males and females differ because of distinctions in parental investment (Trivers). Females would tend to leave the most genes in the next generation by having the best children she can have, as there are frequent limitations on copulation on account of the one-year gestation period. This limits the amount of offspring she can and should have. Males are not limited in this way. The impetus for sex is returned to the male, but only because the male must only ensure he fertilizes as many females as possible, in order to have the most kids. It is also almost a rule that sexually active males outnumber sexually receptive females, leading to high competition for female attention. This means that females are expected to be choosy. Trivers was especially persuaded by a study done by Angus Bateman using Drosophila (Bateman 1948). Bateman was able to conclude that males are more successful the more they have sex, but this promiscuous behavior does little or nothing for female flies (Figure 3). Trivers suggests that male sexual behavior is not limited by gametic formation. Sperm are easy to produce while eggs are not, and so only males have this seemingly inexhaustible supply.
Interestingly enough, the Coolidge effect � which was observed in the lab during animal studies in which males got �bored� with females and could only be rearoused by novel females � was seen by Dewsbury in promiscuous grasshopper mice, which had been thought to be monogamous (Bermant, Dewsbury 1981). In certain cases, females are no better. A study by Olin Bray found that a majority of the clutches of red-wing females from the territories of vasectomized males� territories were fertile, meaning that the females were copulating with some other male red-wing (Bray et al. 1975). Lisle Gibbs, who studied red-wings in Canada, found similar results when DNA-typing chicks across the territorial males� domains (Gibbs 1990). The gels revealed that most of the chicks in any territory were fathered by a different male than the territorial one � and this without any vasectomy. Thus, the tendency to cheat or be promiscuous is supported by both evolutionary theory and practical observation. It is not proven, however, why females are sometimes promiscuous or simply polyandrous � it is hypothesized that it may be fertility insurance, or like humans, merely an artifact of more productive females attracting more males (Birkhead, Figure 3)
As has been shown, it is a mistake to assume that the mother is more �coy� or even the more parental types; in some cases, roles can be reversed with the male. The male magpie, in addition to his copulation role, must also feed his mate and his clutch, thus limiting his promiscuity (Birkhead). This is not in opposition to any part of Trivers� theory � it is just an instance of role reversal, where higher male parental investment ensures higher quality young and thus, his genes into the next generation (Figure 4). As yet, there is no strong logical explanation as to why some species should have the father be the more parental type. Some would hold that the ability to produce milk should dictate the parental unit, delineating one sex over the other. However, there are instances of creatures in which either sex is eminently capable of doing all the important tasks of childrearing. Also, male mammals have the apparatus to produce milk and can sometimes lactate, but they aren�t the main parental unit (Zuk). These differences are mainly assumed to be continuations in evolutionary quirks by selection.
It must be again stressed that the major goal of sexual selection is the maximization of reproductive success or fitness. Courtship, prior to reproduction, is �the advertisement, by a male of how fit he is�genetically. In submitting only to a male with such signs of fitness a female would probably be aiding the survival of her own genes� (Williams 34). While it may be possible, rampant aimless fecundity does nothing for species survival. This is why there are instances of abortions and adoptive societies throughout nature. The kangaroo will expel its joey from its pouch if living conditions deteriorate, just as other mammals can resorb their embryos, birds desert their nests and human parents put their kids up for adoption. Worker bees and ants can give up their reproduction in order to take care of the queen�s offspring. This seems contrary to the genetic preservation inherent in sexual selection; however, it is not. In order to maximize fitness, it may make more sense to discontinue rearing children in harsh conditions and attempting reproduction again later. As for �adoption�, it is not quite clear why so many insects would pass up their own chance at reproductive success. It has been hypothesized that reproducing on one�s own is too unstable and risky such that indirect reproduction through relatives is a much better alternative.
Other species pass up parental care all together in the quest for genetic preservation. Brood parasites, as they are often known, leave their young in other birds� clutches to be raised (Zuk). Cuckoos are especially notorious for this � they are the basis for the term �cuckold� (Birkhead). Another aspect of the vicious struggle present in sexual selection is visible here. As long as the cuckolded parents are raising children not their own, they are lowering their own reproductive success at the same time they are heightening that of the cuckold himself. This form of behavior is very expensive for the cuckolded � but life is tough. Nature isn�t fair, and one should not attempt to apply human visions of justice and morality to these systems.
Geoff Parker elaborated on the presence of the cuckold with his theory of sperm competition (Parker 1970). In this variant on intrasexual selection, sexual selection favors males who can fertilize females who have been previously inseminated by other males. This means that a settled female will raise children with the cuckold�s genes without requiring any other contribution from him. Sperm competition also includes defensive strategies by the paired male and his innate mechanisms to ensure that he will not be cuckolded, or should he be cuckolded, that his sperm should lose out. These include mate guarding, in which a male will essentially follow the female to prevent extra-pair mating attempts; frequent mating attempts; increases in ejaculate and testis size; increasing accuracy of the male reproductive organ; and cooperation among similar sperm, against the activity of alien sperm. The role of the female in all of this is basically unknown. It has been hypothesized that mate guarding is merely a female prompt to ensure the male�s manliness, or find a new mate in somebody else who is willing to stand up to her current mate. Nancy Burley, in studying the zebra finch, found that 80% of all extra pair matings were aggressive, and none of these matings resulted in offspring (Burley et al. 1996). This meant that the female was doing something to avoid bearing the forced embryo � in some species, the female has the ability to eject sperm after a copulation, but the mechanism for this function is unknown.
V. Further Questions and Conclusion
With such variance in mating strategies and fidelity, a major question being addressed in current research is the method by which male and female parents can adjust the amount of energy they expend on raising their offspring when the proportion of offspring from extra-pair males within one clutch can vary from 0 to 90% (Bell). In human contact, the motivations are varied: fear of social reprisal, love or loss of love, socio-economic benefits. With animals, these answers are more obscure. It can be judged how much survival and genetic benefit a female can derive from being with one male or certain males over others, but it is not clear why and how females choose their extra-pair partners. Also, it is not clear why animals should even choose monogamy in the first place. Along with these questions are the more general unanswered questions plaguing evolutionary biology. What are the mechanisms of female choice � are there motivations? Was sex really an adaptation? How did the environment play a role in creating sexual selection? Did most of these adaptations come about as adaptations or as a neutral by-product of selection (Gould and Lewontin)? Are our explanations, however, as neutral as we try to create them, or are we still merely imprinting our life experience on animal society? As science further explores the limitless bounds of evolution, these questions, caveats and exceptions will continually arise in our search for truth.
What science does know about sexual selection is very persuasive. Most scientists are firm with Darwin�s belief in sexual selection and its distinction from natural selection, as are they with his belief in intrasexual and epigamic competition. It is visible in all arenas that there exists a level of same-sex competition for mates as well as a certain amount of choice from the opposite sex.. Furthermore, it is understood that the basic premise on which all selection stands is the passing on of genes � so the ultimate goal of reproduction is the extension of genetic heritage into future generations. Observations of social behavior tend to prove the existence of mating strategies for specific characteristics that have tended to be over-promoted in species, over survival selection pressures. The theories of Zahavi, Fisher, Parker and Trivers are very reasonable and make sense within the context of what science knows about sexual evolution, but, as in all sciences, one must be very careful of wholly accepting what is still theory and not entirely proven fact. Hopefully, with further research, science will be able to answer all that is necessary to know to understand why animals � and us as human in general � have developed this way, and how.
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