I think just taking the one bit of sexual selection, that men need to spread their seed, is just far too simplistic, and it a gross mis-interpretation of evolutionary biology.
If you are a Christian and don't believe in evolution, then using any of these evolutionary arguments to justify 'males just naturally want to shag about' is a non-starter.
I will be watching out for you
http://technology.newscientist.com/article/mg12517003.800
DARWIN'S theory of natural selection explained, at a single blow, the evolution of all sorts of adaptations that enhance an animal's ability to survive. But he was puzzled by behaviours and anatomical features that do nothing to increase survival, and that may even hamper it. Darwin concluded that features such as the peacock's tail and the Irish elk's antlers, characteristics usually sported only by males, evolve by a different process, which he called sexual selection. His idea was that these characters evolve because individuals possessing them acquire more mates than their competitors of the same sex. Darwin suggested that sexual selection favours the evolution of such characters in two ways. The most obvious is direct competition among males for mates, involving aggressive clashes of horns and antlers. A more subtle mechanism is the preference of females for certain males as mates - the peacock with the biggest, glossiest tail feathers, say. The males that succeed in competition and are most attractive to females acquire more mates and sire more offspring than less successful or less well-endowed males.
In developing his theory of sexual selection, Darwin realised that males tend to court females and compete with their rivals, while females are coy and choosy when it comes to reproduction. However, he was unaware of the biological reason for this common difference between the sexes. Our understanding of this aspect of sexual selection came 100 years after Darwin published The Descent of Man and Selection in Relation to Sex, thanks to the work of Robert Trivers of the University of California at Santa Cruz. Trivers argued that, although both sexes attempt to pass as many copies of their genes to the next generation as possible, females and males have evolved different tactics to achieve this same end.
Typically, a female produces much larger and many fewer eggs than a male produces sperm. A female has only a limited number of eggs available for fertilisation during an episode of reproduction, and so she has little to gain from mating with many males; a single mating may provide a female with all the sperm she needs. However, a female may gain an advantage by being choosy about which male she allows to fertilise her eggs, preferring, say, a genetically superior male or one likely to be a good father. The situation is just the reverse for a male, whose genetic contribution to the next generation is limited largely by the number of eggs he can fertilise. For males, the optimal tactic for passing on genes is to mate with as many females as possible.
So in general, males gain more from indiscriminate and frequent mating than do females. Darwin's theory of sexual selection does not predict that males should choose mates; indeed, we may even predict that they will not do this, given that choosing a mate from an array of potential partners takes time and effort which could be spent doing other things, such as acquiring further partners. If males have opportunities for mating several times, any benefit to being choosy could be outweighed by the cost of missed opportunities for further matings.
Yet evidence is growing that males of many species may invest heavily in each mating episode in a way that decreases their ability to invest effectively in further matings. Under this circumstance, the cost-benefit balance may favour males who choose their mates. A number of factors, acting alone or in combination, may cause such a shift by limiting opportunities for males to mate many times.
Received wisdom has it that males can produce almost limitless supplies of sperm. While it is certainly true that males produce more sperm than females produce eggs, biologists are now discovering that ejaculates, spermatophores or even spermatozoa themselves are in limited supply. This seems to be true in organisms as diverse as insects, fishes, amphibians, birds and mammals. For example, males of many species of salamander living in temperate regions produce mature sperm between, but not during, mating seasons. Thus, a male begins each season with a fixed amount of sperm that he has to partition between spermatophores, which in turn are partitioned among mating partners. Supplies are limited even in species in which males are constantly producing sperm. In rats, the sperm counts and ejaculate volumes decline as the frequency of copulation increases, and a female is less likelyto become pregnant if her partner has already ejaculated KK several times. Even if numbers of sperm are not severelylimited, males may need time between successive matings in order to re-synthesise the various components that form the medium in which sperm are transferred. In salamanders, this period of recovery lasts as long as three days.
As Darwin recognised, it is usually the male, not the female, that invests time and energy in advertising or searching for mates. Such investment limits the amount of time left for other activities, such as feeding. Attracting females can also be costly in terms of energy. For example, male frogs andtoads that call to attract females may lose weight during thebreeding season.
An advertising or searching male pays the greatest cost if he encounters a predator or parasite rather than a mate. A rather bizarre example of this occurs in certain male fireflies that produce bioluminescent flashes to seek out females. When a female of the male's species sees his flash, she signals her presence by flashing back and this may lead to mating. Females of other, predatory species, however, also respond by flashing to males. As James Lloyd of the University of Florida at Gainesville has found, such firefly 'femmes fatales' devour males attracted to them. The combined costs in terms of energy expended and the risk of predation are considerable in many species. These costs may severely reduce a male's chance of mating many times.
Males may transfer more than just sperm to females at the time of mating. In many insects and some birds, females accept males as mates only if the males offer them an item of food, known as a nuptial gift. Collecting such a gift may be as hazardous for males as searching for a female. For example, male scorpion flies are allowed to mate successfully only if they offer females large, palatable nuptial gifts of insect prey; females rely heavily on nuptial gifts as they do little hunting for themselves. Males searching for such gifts may, however, become entangled in the webs of predatory spiders. In many insects, the ejaculates or spermatophores of males contain energy-rich nutrients as well as sperm. Experiments with radioactively labelled spermatophores have demonstrated that females use these nutrients in the production of eggs. In many butterflies, males can acquire these nutrients only during their lives as larvae. The non-renewable nature of these materials may limit further mating opportunities for males. And, even if the nutrients are renewable, males may need time between matings to replenish their supplies.
Beauty and the beast
So males of many species often experience heavy costs associated with mating. How might they be choosy in their mates? A preference for females that appear to be free of disease might benefit a male in several ways. In a direct manner, choosy males may avoid becoming infected with a disease themselves. Less directly, females infected with disease-causing organisms may be less fertile, produce fewer offspring, or be less competent as mothers as a consequence of their infection.
Animals may also enhance their offspring's chances by opting for partners that strike them as slightly unfamiliar. As is well known to animal breeders, offspring produced by close relatives in species which normally do not inbreed are frequently inferior to offspring produced by less-closely related partners. Animals in natural populations avoid this effect, known as inbreeding depression, in a number of different ways. Relatives of one sex may tend to move away and reproduce some distance away from the other sex, so reducing the average degree of relatedness between mates. With some exceptions, females disperse from their natal groups among birds, while males are the main dispersers in mammals.
Even when animals do not disperse, they may avoid inbreeding by choosing unrelated or novel partners. For example, in wild horses, females usually leave the harems into which they are born. But in those cases where females do not leave but reach maturity in the presence of male relatives, fathers and even stepfathers are unlikely to attempt to mate with their daughters and stepdaughters. Familiarity leads to disinterest at the time of mating.
In many species of fishes, birds and mammals, the growing young learn the key characters that are typical of the species to which they belong, a process known as sexual imprinting. For example, in a brood of mallard ducks, males learn the characteristic plumage of females of their species from their mother and sisters. Female chicks cannot learn the plumage typical of the male, because their father is not present and their brothers possess juvenile, not adult, plumage. Early learning ensures that, when mature male mallards attempt to copulate they do so only with females of their own species. Another type of learning during early family life may ensure that the young learn to discriminate their kin from unrelated individuals. In some species, such early experience greatly influences later preferences for mates. Japanese quail, for instance, prefer partners who are neither too closely related nor completely unrelated; both males and females prefer first cousins as partners. Such a preference leads to what Patrick Bateson of the University of Cambridge has called 'optimal outbreeding', and results in a balance between the harmful consequences of inbreeding and harmful effects that might happen if excessive outbreeding disrupts complexes of genes that confer adaptation to particular local environments.
Males can also choose females in an attempt to ensure their paternity. Females may mate several times to replenish exhausted sperm supplies or to obtain nutrients which males transfer at mating. But this creates a quandary for males: it can lead to a situation known as sperm competition, in which sperm from several males compete in the female's reproductive tract for fertilisation of the eggs. Geoffrey Parker of the University of Liverpool has suggested that such sperm competition is a potent force in the evolution of the mating tactics of males, each struggling to ensure that his sperm will fertilise a female's eggs.
One such tactic on the part of males is to mate preferentially with females that have not mated previously. In many butterflies, males spend more time courting females that are both young and large. Young females are unlikely to have already mated, and larger ones bear more eggs for fertilisation than smaller females. Males assess the age of females by the amount of wear on their wings, which increases as females age. In some mites, a preference for unmated females has led to a curious mating tactic in which males guard immature females, mating with them once the nymphs develop into mature females. Such guarding represents a considerable investment of time, decreasing the number of females with which a male can mate over time. To minimise this investment, males preferentially guard those female nymphs that are closestto maturity.
Male preferences for unmated over mated females have been explored intensively among rodents studied in captivity by Donald Dewsbury and his colleagues at the University of Florida at Gainesville. Male prairie voles are more discriminating than male montane voles; the prairie voles spend more time investigating and copulating with unmated females. This species difference in male preference seems to be related to differences in the extent to which males invest in reproduction. Prairie voles appear to live as monogamous pairs in nature, while montane voles are more promiscuous. That male prairie voles should be more discriminating is not surprising as monogamy self-evidently reduces opportunities for multiple mating. In addition, preferring an unmated female increases the chances that a male prairie vole will invest paternally in his own offspring, not those of another male.
In promiscuous species in which males and females remain together only for as long as it takes to mate, males gain little by mating repeatedly with the same partner. Indeed, such matings are likely to be costly, if only because they take time to complete, time that could be spent pursuing other females. In many species, a male apparently loses interest in a female once he has mated with her. This is not because the male is unable to mate again, for if he is given a novel female, he will resume sexual activity. This effect of novel females has long been exploited by breeders of cattle, where, for example, bulls will maintain high rates of ejaculation if presented with a succession of different females. This phenomenon is known as the Coolidge effect after an American president, Calvin Coolidge. The story goes that, on a visit to the chicken house of a government farm, Mrs Coolidge asked the farm manager how many times a rooster mates. When told that roosters mate dozens of times a day, Mrs Coolidge asked the manager to tell her husband of the males' prodigious ability. When asked by President Coolidge if the cocks were exposed to the same females, the manager told him that different females were used. 'Tell that to my wife,' said President Coolidge. Whether this story is true or not, a consequence of the Coolidge effect is that the male distributes his sperm (and his genes) over a number of different females.
Dewsbury recently analysed the published literature on the Coolidge effect. His critical review suggests that the effects of novelty depend very much on how the animals were tested in the laboratory. He also found a great deal of variability among species in the ability of novel females to reawaken the mating behaviour of males. Dewsbury and his colleagues suggest that such variation may reflect differing opportunities for males to mate repeatedly in the wild. Species that form monogamous pairs have no need for the Coolidge effect, as opportunities for multiple matings will obviously be limited. In preliminary studies, Dewsbury and his colleagues have found more evidence for this view. The novelty of females has no effect on the mating behaviour of males in old field mice and prairie voles, believed to be monogamous species. But the Coolidge effect does seem to operate in deer mice, montane voles, meadow voles and rice rats, all of which are more promiscuous in their mating habits.
Better understood is the effect of cycles of female sexual responsiveness on the mating tactics of males. In mammals, mating is most likely to result in fertilisation and conception at the peak of the oestrous cycle, a phase known as oestrus. Females may signal when they are in oestrus in a number of ways, and males respond by altering their attentions. In troops of savanna baboon of Africa, for instance, studied by Glenn Hausfater of the University of Missouri, the most socially dominant males express sexual interest only in females that signal they are in oestrus by changes in the degree of swelling in their sexual skin. Top males tolerate matings by less dominant males in the troop except on the crucial day of the cycle, at which time the most dominant male is most likely to consort with the female. This preference ensures that the alpha male mates at the time in the oestrous cycle when fertilisation is most likely.
Males may also choose females on the basis of their reproductive powers. In many primate species, older females who have already produced offspring are more successful in future reproductive attempts than adolescent females or young females who have not yet produced young, and males frequently prefer such older, experienced females. For example, adult males in wild groups of chacma baboons ignore sexual invitations from adolescent females, but will mate readily with older females. Female size, amount of body fat, size of the sexual swelling on the rump or even the appearance of the nipples may be signals that males use to assess female age and past reproductive performance.
Even if all of the females in a population are equally fertile, they may vary in 'fecundity' - in the number of offspring they can produce during any one reproductive episode. In many insects, fishes and amphibians, the volume of a female's body cavity constrains the number of eggs she can produce. In general, a large body can hold more eggs than a small body. A preference for larger, more fecund females is perhaps the most common manifestation of mate choice among males of many insects, and in a number of fishes and aphibians.
In some species of fish, especially those that live in coastal or fresh waters, the male not only selects the spawning site but also protects the developing embryos. Because these males invest time and energy in caring for the young, it makes sense that they should often prefer larger, more fecund females. But despite their paternal attentions, males may still be able to engage in further matings while they have embryos. Indeed, for male sticklebacks defending especially good territories, the presence of eggs may make them even more attractive to females. Pipefish are close relatives of the sea horses, and in both groups, males care for the offspring, nursing their young in a brood pouch and transferring nutrients to them. Like the stickleback, male pipefish prefer larger females, but their opportunities for multiple mating may be constrained by the size of the pouch in which embryos develop.
Male preference for larger females may result in a pattern of mating described as 'size-assortative'. In this pattern, large males tend to be paired with large females, small males with small females. Mark Ridley, then at the University of Cambridge, suggested that this pattern of mating is most likely when large females are more fecund, large males are better competitors than smaller males and when pairs remain together for some time. Size-assortative pairing has been described in many arthropods, such as the freshwater shrimp Asellus. In this crustacean, males physically guard females until they moult; only then is fertilisation possible. Male Asellus not only prefer larger, more fecund females as mates, but also prefer females which are closest to moulting, thus decreasing the amount of time they invest in each mating episode. Because only large males can compete successfully for preferred females, mating patterns are size-assortative.
Mating opportunities may be limited when males provide care to their offspring, perhaps because they simply are unable to gain access to other females, or because females find these males unattractive. In species in which both the male and female provide care for their offspring, males may choose mates on the competence of their partner as a mother. In the higher vertebrates, monogamy - a more-or-less permanent bond between individual males and females - is most common among birds; over 90 per cent of subfamilies of birds are apparently monogamous. North American pinyon jays form monogamous pairs in which the male invests heavily in his offspring. A complex system of mating preferences exists in both sexes. Males prefer larger, old females that are probably experienced breeders. Such a preference is likely to be advantageous as it may lead to early breeding. Complex patterns of mate choice also exist in the feral pigeon, in which both the male and female care for offspring. Nancy Burley of the University of Illinois at Champaign found that both sexes are choosy concerning mates, although females are choosier than males. Plumage colour, age and breeding experience are important criteria for both sexes.
In monogamous birds, reproductive performance tends to improve as the members of a pair gain greater experience of one another over several seasons. In the kittiwake gull, for example, retention of the same mate from one breeding season to the next results in a 12 per cent increase in the number of chicks fledged per pair. 'Divorce' in kittiwakes is most common after a previous breeding attempt has failed. But the extent to which males of this species actively choose to stay with mates is uncertain, for the territorial behaviour of males at the nesting colony severely reduces the number of females to choose from.
So we see that mate choice of females by males is not uncommon in the animal kingdom. It seems to occur wherever the benefits to being choosy outweigh the costs, a situation that is most likely when males have limited opportunities for multiple mating. The best evidence for the existence of choosy males has come from experimental studies in the laboratory where researchers controlled for the effects of female choice and competition among males. But detecting mate choice by males in nature is likely to be no easy task.
To complicate the task, the expression of male mate choice, even in a single species, may vary in both time and space. For instance, Darryl Gwynne of the University of Toronto found in a study of Mormon crickets that at low densities, males compete fiercely for females and show no evidence of choosing mates. But when population densities of the crickets are high, males prefer more fecund females. The balance shifts to favour male choice because at high densities food tends to be scarce, so nutrients transferred in male spermatophores become very important to females. Indeed, in such circumstances females compete with one another for access to males and their nutritious spermatophores.
Darwin was not wrong when he characterised males as competitive and females as choosy. But we now know that males can and do mate preferentially with certain females when the time and place are right.
* * *
How do humans choose their mates?
THE FACT that human beings neither mate nor marry at random has attracted considerable attention from sociologists, psychologists, anthropologists and biologists. Attempts to understand the decisions and choices that underlie human attraction and marriage fall broadly into one of two approaches which I call 'psychosocial' and 'sociobiological'.
The psychosocial approach typically seeks to determine the extent to which partners match on a number of sociological, psychological and physical measures. In general, similarities between partners are more common than differences. Partners tend to resemble one another in age, height, weight, eye colour, overall physical attractiveness and even the length of their ear lobes. Ethnic background, religious affiliation, educational background, opinions about current affairs and a variety of personality scores also tend to be similar. There is even evidence for similarity between spouses in psychiatric disturbances, such as schizophrenia. Of course, not all of these characters are truly independent of one another; tall people tend to be heavier, and members of a certain ethnic background often share religious affiliation.
Do men and women choose similar qualities in their partners? In a study designed to answer this question, men and women were asked to rank certain characteristics of a potential partner from most to least preferred. Both men and women agreed that characteristics such as honesty, kindness and understanding are most desirable. Women gave a higher ranking to good earning capacity than did men, whereas the reverse was true for physical attractiveness. One large-scale study of married couples found that attractive women are often married to men with higher incomes.
The extent to which similarities between partners represent the results of a choice of mate is unclear in many studies. For example, partners in long-term relationships may appear similar due to convergence in certain personality traits over time. In addition, similarity may reflect a limited choice due to the spatial distribution of members of the opposite sex. For example, one study found that the average distance between the birth place of husband and wife and the place where they were married was only 177 kilometres. Finally, in societies in which marriages are arranged, similarities between spouses may reflect decisions taken by family members rather than by the spouses themselves.
The psychosocial approach to the study of mate choice outlined above has been criticised because it often regards choice as a rather static event, in which more-or-less instantaneous decisions are made based on some certain characteristic, or set of characteristics. Another, and perhaps more realistic, way of looking at mate choice is to treat it as a dynamic process in which partners communicate and negotiate to produce a desirable relationship. Studies in which the choice of mates is seen as a dynamic process have revealed that similarities and differences between partners are often highly complex, can vary from couple to couple and can change over time as relationships mature.
The sociobiological approach is championed most fervently by Edward Wilson of Harvard University in Boston and is based on the belief that human social behaviour has evolved in the same way as that of other animals, and for the same reasons. Many sociobiologists start by predicting howindividual humans should behave in orderto maximise their survival and reproductive success. Then, the researchers examine human social behaviour to see if what they observe matches what they had predicted. Sociobiologists believe that our genes bias our sexual behaviour so that we act in ways that increase our reproductive success.
Much has been written both for and against the sociobiological approach to human behaviour, and many workers have attempted to understand human reproductive tactics in the light of Darwin's theory of sexual selection. In its simplest (and most naive) form, sociobiology predicts that women will be choosy concerning who they accept as mates, preferring and remaining faithful to the men who control the resources they need to rear their children successfully. Men are predicted to compete among one another to obtain both women and the resources they require, and promiscuously father as many children as they can.
From the point of view of the human male, we can make sociobiological speculations a little more realistic. Because men do invest in their offspring and may sacrifice opportunities to mate with many females in order to be good providers, we might predict that men will exercise some degree of mate choice. Sexual jealousy in men and the high value placed on female virginity in many societies (and its associated trappings, such as veiling and infibulation) can be interpreted as manifestations of male preference for women that bring with them a high certainty of paternity. Marriage itself can be seen as a tactic by which men sequester women to control their sexuality and guard them from the attentions of other men and the risk of infidelity.
As sociobiologists, we might predict that men should not only prefer virgins, but also women of high fertility. The behaviour of the Kipsigis tribe of Kenya appears to fulfil this prediction; in that society men must make a payment to a woman's family before marriage (in a cross-cultural survey of 860 human societies, a man or his family pays for a wife in almost 70 per cent). Kipsigis men pay the highest amounts for women who reach puberty early, and these women produce more surviving children over their lifetimes than do women who reach puberty at later ages.
Yet the fact that aspects of human sexual behaviour match the predictions of sociobiological theory does not mean that this approach is correct. Often the theory rests on scientifically untested (and sometimes untestable) assumptions and, because of its evolutionary nature, depends on unknowable facts about the lives of our ancestors. It is true that we should not deny the evolutionary heritage behind our behaviour. But it is also true that, no matter how plausible evolutionary explanations about human behaviour may be, they require the same rigorous scientific treatment as is given to any other type of explanation. In human sexuality, our biological heritage as well as more recent cultural factors are likely to interact in complex and fascinating ways.
Dr Paul Verrell is an ethologist at the University of Chicago.
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