Sexual Selection: Darwin, Mate Choice & Behaviour - PDF

3 Sexual Selection Key Concepts sexual selection female choice parental investment handicap hypothesis parasite theory Muller’s ratchet tangled bank the Red Queen arms race androphilia gynephilia Natural selection has become well accepted as the main mechanism of evo...

3 Sexual Selection Key Concepts sexual selection female choice parental investment handicap hypothesis parasite theory Muller’s ratchet tangled bank the Red Queen arms race androphilia gynephilia Natural selection has become well accepted as the main mechanism of evolutionary change. Despite this acceptance, it is clear that it fails to explain why males and females of many species differ so much. In this chapter we consider the way that the behaviour of each sex might affect the behaviour of the other. This is the concept of sexual selection. We also consider why sex itself exists as a means of reproduction when so many species are able to do without it. Finally, we look at some examples from the animal kingdom of how the behaviour of each sex may be affected by sexual selection. Darwin and Sexual Selection During the writing of The Origin of Species Darwin realised that many animals had both physical and behavioural features which are very difficult to explain in terms of natural selection. Because they face the same ecological pressures, natural selection should drive the characteristics of males and females of a species in the same direction; and yet in many vertebrate species males are larger and more gaudy than their female counterparts. Furthermore, males generally engage in a greater degree of risk-taking behaviour. The elaborate feathers that make up a peacock’s tail, for example, make him conspicuous to predators such as foxes and tigers and the piercing calls that he makes to attract females also inform predators of his whereabouts (Miklósi and Konok, 2020; Prum, 2018). Since natural selection was thought to promote anti-predator adaptations, it seems strange that such features should have arisen in his ancestors. In addition to drawing attention from predators, the time and energy that many males spend in making courtship calls might otherwise have been spent on foraging and on other ben- eficial activities such as preening. This means that being attractive to females and spending time attempting to attract them must have real and potential costs. Despite these costs Darwin realised that traits which helped males to attract females would increase their chances of mating and thereby of passing on such features. So Darwin argued that features which helped you to breed might par- adoxically sometimes be selected for, even up to the point of shortening your life. In 1871 with the publication of The Descent of Man, and Selection in Relation to Sex he developed a new selective force, sexual selection. Sexual selection applies to those characteristics that provide individuals with advantages in gaining access to mates (Prum, 2012; 2018). Hence if natural selection is sur- vival of the fittest then we can think of sexual selection as ‘survival of the sexiest’. Evolutionary 56 Sexual Selection psychologists have suggested that this is as true of our species as it is of others (Barkow, 1989). A number of surveys of human mate preference, for example, demonstrate how men from a wide range of cultures find the classic hour-glass shape of young women particularly attractive (Buss, 2019; Buss and Schmidt, 2019). This makes sense when applying sexual selection theory since this shape is an indicator of fertility in women (human mate preferences will be discussed further in Chapter 4). Intrasexual and Intersexual Selection Having introduced sexual selection in The Descent of Man, Darwin went on to outline how this competition for mates might take two different forms. Intrasexual selection consists of individ- uals competing with members of their own sex for access to the opposite sex. In most cases this means males fighting with each other for access to females. In contrast, intersexual selection consists of members of one sex attempting to impress members of the other; in this case the em- phasis is on females since they are generally the ones that need to be impressed before they will assent to mating. Intrasexual selection is generally regarded as being responsible for males de- veloping weapons to compete with each other such as large teeth and horns, greater musculature and a lower threshold for aggression when compared to their female counterparts (Clutton-Brock et al., 1982; Zuk and Simmons, 2018). Intersexual selection, however, is believed to lead to the evolution of sexual ornamentation such as brighter plumage and courtship display in males in order to impress females (Andersson, 1982; Brennan, 2010). For their part, Darwin predicted that females should be choosy about which males they accept as mating partners, perhaps discrimi- nating on the basis of male ornamentation and display. This means that for most species we can equate intrasexual selection with male–male competition and intersexual selection with female choice. Do Females Have a Choice? In contrast to natural selection, the notion of sexual selection did not receive strong support during Darwin’s day, even from those within the biological fraternity. While there was some acceptance that males might develop weapons such as tusks to compete with each other over females, many experts were distinctly sceptical about the idea of female choice. Given that females are smaller and less ag- gressive than males in most species, surely they were unlikely to have much choice when it came to sexual matters? In addition to this practical argument there were more serious theoretical concerns. In particular, Darwin was unable to explain why female preference should arise. Many examples of male adornment and courtship rituals were known to nineteenth-century naturalists, from the gaudy face of the mandrill (see Figure 3.1) to the exotic feathers of the birds of paradise. Although it might be argued that males which were successful in using such features to attract females would pass on such characteristics to their offspring, this still raised the question – what was in it for the females? Why should they choose gaudy males who would surely attract greater attention from predators? During the twentieth century a number of theories were advanced which attempted to answer these questions (Hydr, 2009; Zuk and Simmons, 2018). It is useful to explore these theories in order to understand how sexual selection has gradually become of great importance to the understanding of the relationship between evolution and behaviour.  Theories of Sexual Selection 57 Figure 3.1 Display of dominant male mandrill. Box 3.1 Two Forms of Selection or One? From the moment Darwin introduced the notion of sexual selection into biology there has been a long-standing debate as to whether it really is a distinct and separate process from natural selection. Since each leads ultimately to increasing inclusive fitness (see Chapter 2), then might they not both be labelled ‘natural selection’? And, even for those who accept the argument of two separate processes, there remains one specific sticking point. Male weapons, such as enlarged teeth and horns, are frequently used to fight with each other and to ward off predators. This means that it is not always easy to determine the extent to which sexual and natural selection have contributed to the development of these features (Halliday, 1994). However, given that many examples of gaudy male ornamentation are likely to be driven in different directions by natural and sexual selection, we feel it is instructive to consider the two processes separately. Theories of Sexual Selection Sexy Males and Parental Investment In 1930 the English geneticist Ronald Fisher turned his attention to the relationship between female choice and male adornment and in doing so he rekindled interest in sexual selection. Fisher (1930) argued that ancestral females would have been attracted to males which had, for example, well- 58 Sexual Selection maintained tail feathers, since these might signal that they are likely to be good flyers. Furthermore, since such males had time to maintain such feathers, this was evidence of superior foraging and other abilities that would aid survival. For Fisher the feature chosen by females had to have some original survival advantage. Once the tail feathers (or whichever feature) had been selected, however, they could become exaggerated and evolve beyond their original function. Females who preferen- tially mate with males which show these inherited attractive features will, of course, produce more attractive sons since their offspring are likely to have the genes for such characteristics. Such sons would also be more likely to be chosen by females in the future. To Fisher, then, the most important trait that a male can offer a potential mate is his genes for being attractive. This suggests that once a feature has been chosen by females it may become progressively exaggerated with each generation since females will constantly be looking for individuals with the largest, brightest example of that feature. Fisher called this ‘runaway selection’ since the feature runs away from its original function and becomes selected purely on the basis of its attractive qualities. In this way Fisher was able to put forward an explanation for the extreme tail feathers that we see today in peacocks. Eventually, according to Fisher, such superplumage would stop being exaggerated further because of its costs to survival; natural selection would therefore keep runaway selection in check. That is, there will be a trade-off between attracting females and costs such as attracting predators (Zuk and Simmons, 2018). Parental Investment Despite Fisher’s efforts in this area, there was still an important piece missing from the theory. Dar- win assumed that males would compete with each other for female attention and that females would be the choosy ones. But why should this be the case rather than the reverse? In 1972 Robert Trivers suggested that sexual selection is directly related to asymmetries between the sexes in the amount of effort that each parent puts into raising the offspring. He called this effort parental investment. Triv- ers (1972; 1985) chronicled the various ways that, for the vast majority of animal species, females invest a great deal more effort into producing offspring than do males. This asymmetry begins with gamete formation where males produce a large amount of low-cost sperm compared to the relatively small number of larger and more expensive eggs produced by females. Since an egg contains the material that provides for the initial development of the zygote it is approximately 1 million times larger than the spermatozoan that fertilises it. In contrast, a sperm provides nothing more than its genes. For most species this disparity of numbers means that, while females are limited in having a comparatively small number of eggs that may be fertilised during their lives, males are limited only by the number of matings they are able to accomplish. Asymmetrical gamete cost, however, is only the beginning of the inequality of investment between the sexes, since females generally put more time and effort into the rearing process. For mammals, this sexual disparity in effort can be enormous owing to the role that a female plays in terms of gestation, lactation and general nurturing. Since females invest so much in their offspring, Trivers argued that they should be very choosy about which males they allow to fertilise their eggs. For males, however, where the costs of reproducing are nearly always lower, Trivers predicted there should be far less discrimination and choosiness. A male that makes a poor mating choice loses very little (frequently no more than a little effort and a small amount of sperm). A female who makes a bad choice, however, will generally have to pay a much heavier cost for her mistake because she is generally the one left ‘holding the baby’. An extreme example of this sexual asymmetry is illustrated by the differing reproductive efforts made by male and female elephant seals (Trivers, 1985; Sanvito et al., 2007). Male elephant  Parental Investment 59 Figure 3.2 A male elephant seal dwarfs the surrounding female and pups. Figure 3.3 Harem size in relation to size of male. seals (bulls) weigh in at almost 3000 kg; females (cows), in contrast, are about a quarter of this size – typically around 650 kg (see Figures 3.2 and 3.3). A bull elephant seal provides a few grams of sperm while the cow typically produces a pup weighing around 50 kg. During its first five weeks of life the pup will gain 100 kg and the cow will lose 200 kg. In contrast, the male puts his time and effort into inseminating as many other females as possible and defending his right to do so by threatening and fighting other males.  60 Sexual Selection So, 100 years after Darwin first proposed the mechanism of sexual selection, Trivers suggested that choosiness in females is a direct result of their greater investment in offspring. Following Trivers’ watershed paper of 1972, students of animal behaviour have paid more atten- tion to the notion of female choosiness and its relationship to male traits. The repercussions of female choice are interesting when looking at characteristics in males. Is it possible that many present-day male characteristics may be the direct result of choices that their female ancestors made? Female Choice and Male Adornment Most of the work on sexual selection since Trivers’ paper on parental investment has been con- cerned with how females are able to assess a male’s quality (Manning and Stamp-Dawkins, 2012; Zuk and Simmons, 2018). One of the most controversial ideas came from the Israeli evolutionist Amotz Zahavi, who turned Fisher’s idea on its head. Zahavi (1975) suggested that males might develop ornaments not to look attractive but, perversely, as an impediment in order to demonstrate their abilities to survive despite having such a handicap. According to this argument, males develop elaborate ornaments in order to signal ‘I must be a good quality male if I can survive carrying this burden!’ Hence to Zahavi male adornments allow females to assess their ability to survive and hence they are real signals of genetic quality. As with Darwin’s original notion of sexual selection, despite initial criticism (e.g. Maynard Smith, 1978), what has become known as the handicap hypothesis has subsequently gained support from a number of experts (e.g. Andersson, 1986; Grafen, 1990; see also Zahavi, 2003). Table 3.1 Theories of evolutionary origin of male characteristics Theory and associated Theory proposes Theory predicts researcher Runaway selection theory Male adornments driven beyond Females will choose males purely on (Fisher, 1930) original function by female grounds of attractiveness preference for attractive features Male features not direct indicators of genetic superiority, i.e. ‘sexy sons’ Parasite theory (Hamilton Male adornments arose to display lack Females choose male features that and Zuk, 1982) of parasites to females demonstrate a lack of parasites and hence genetic quality Male features signify genetic superiority, i.e. ‘healthy offspring’ Handicap theory (Zahavi, Male adornments are chosen by Females choose males which show 1975) females for their conspicuous and conspicuous and costly adornments costly nature as a sign of genetic quality Male features signify genetic superiority, i.e. ‘healthy offspring’  The Parasite Theory and Honest Signalling 61 The Parasite Theory and Honest Signalling In a similar vein to Zahavi, but somewhat in contrast to Fisher’s argument, in 1982 Bill Hamilton and his colleague Marlene Zuk proposed that male adornments evolved to demonstrate to females that they are free from parasites. They call this the parasite theory of female choice. Parasites, of course, may be anything from tapeworms and fleas to microbial life forms such as bacteria and viruses. Given that parasites account for a larger proportion of fatalities than either predators or competitive conspecifics, so the argument goes, males which develop an elaborate healthy feature should be chosen by females since they are likely to pass on healthy genes to their offspring. To put it another way, if males with the fewest parasites are able to produce the most elaborate ornaments and if females choose males on this basis then they should be passing disease resistance on to their offspring. The parasite theory differs from that of Zahavi in that, while both rely on males offering real signals of quality, the ornament is seen as a development to display health directly rather than as a handicap. The implication is clear, the more parasites have played an important role in your an- cestry then the greater the pressure on you to signal your lack of them. The Hamilton–Zuk parasite theory raises a fundamental question about the signals that animals give to each other. In order for this theory to stand up it is necessary for males to be honest signallers. This means that, for females to benefit from the signals that male ornaments provide, it is necessary that these features really do correlate with parasite resistance rather than simply appearing to do so. Evaluating Theories on Female Choice and Male Adornment Although the Hamilton–Zuk theory has been received favourably in recent years it is by no means universally accepted and there is still much debate surrounding sexual selection theory. Currently, the main sticking point is whether males’ ornamentation has evolved simply to make them attractive to females or whether it serves as a signal of real quality. The former argument can be traced back to Fisher, while the latter is currently supported by the Hamilton–Zuk parasite theory. Matt Ridley (1993) refers to this debate as the ‘Fisherians’ versus ‘good-geners’, although it has also been called ‘sexy sons’ versus ‘healthy offspring’ (see Cronin, 1991). For the ‘good-geners’ it is necessary to demonstrate that male adornments are widespread real signals of health and disease resistance in the animal kingdom. For the ‘Fisherians’ it is necessary to demonstrate that females favour males purely for their attractive features – their ‘sexiness’ – which a female can then pass on to her sons. Currently both sides can claim some support from the experimental literature (see Box 3.2). The studies outlined in Box 3.2 are certainly consistent with the notion of parasites having played a role in male adornment, but they are not direct evidence of female choice. Might not male– male competition have provided the driving force for such plumage rather than female choice? Today there is quite clear evidence that female choice is involved in the development of male adorn- ments. In swallows, for example, it is well established that females prefer males with longer tail feathers (Moller, 1988; 1990). This finding, in isolation, might be taken as evidence for either a Fisherian or a good-genes argument (Moller himself favours Zahavi’s handicap hypothesis, which is a form of good-geners argument). In 1994, however, Norberg decided to determine whether or not male swallow tail feathers are a direct signal of a healthy feature or just a signal of sexiness (see Figure 3.4). He placed a number of male swallows in a wind tunnel and discovered that those with 62 Sexual Selection Figure 3.4 A male barn swallow’s long tail is a sign of good health and is attractive to females. longer tail feathers had improved flight performance due to an increase in lift. This suggests that the long tail feathers not only increase the attractiveness of a male but that they may do so because they are a real and direct indication of good genes. That is, they aid the development of an aerodynami- cally superior tail despite ecological pressures such as the presence of parasites. Box 3.2 Fisher versus Hamilton–Zuk – Attractiveness versus Good Genes One area of study, which appears to support Fisher’s runaway selection hypothesis concerns sensory bias in females. Female sensory bias means that they pay particular attention to specific male features and that such an attention bias is inherited as a part of sexual selection. Basolo (1990) demonstrated, unsurprisingly, that female swordtail fish prefer males with the longest sword (an extension of the tail fin which only males of the species have). This would be predicted by both Fisherians and good-geners. What is surprising, however, was the finding that females of a closely related species called platyfish, a species in which neither sex has a sword, also prefer males with a long sword. In other words, these females prefer males of another species because they have the same sensory bias as their close relatives. The explanation for this curious favour- itism appears to be that male platyfish used to have a sword, which they lost quite recently in evolutionary terms; but females still have the sensory bias for this feature (Basolo, 1995). Basolo suggests that the sword of swordtail fish does not signal a real health benefit but that it is simply a sexy male feature.  The Parasite Theory and Honest Signalling 63 Box 3.2 (cont.) But surely if female platyfish currently have a sensory bias for a sword-like tail how can we explain its loss in the males of their own species? Haines and Gould (1994) may have provided the answer by studying a relative of both swordtails and platyfish – guppies. They found that guppies with shorter tails were better able to escape from an artificial predator than those with longer ones, despite the fact that females preferred the longer-tailed males! Perhaps the ancestors of each of these three related species had to solve different problems of predator pressure? Fol- lowing an initial female preference for long tails in the common ancestor of all three species of fish, perhaps platyfish and guppies moved to areas where, due to specific predator pressure, the benefit of a shorter tail outweighed the advantages of having a sexy long tail. This scenario may be a good illustration of how natural and sexual selection may pull in different directions and how males might have to make compromises. If Basolo’s studies appear to lend support to the Fisherians, the good-geners can also draw on a number of studies to back their own stance. Zuk (1992), for example, has demonstrated that in tropical birds, the number of parasites a species has is directly proportional to the greater the degree of ornamentation seen in its males. Furthermore, it also appears that it is only those males who really have resistance to parasites that are able to produce the most striking orna- ments (Zuk, 1992). Indeed it is now known that in a wide range of species including fishes, frogs, insects and birds it is the flamboyant species that are particularly troubled by parasites and within these species females show a clear preference for males which have the fewest parasites (see Cronin, 1991; Ridley, 1993; Willis and Poulin, 2000; Martin and Johnsen, 2007; Zuk and Simmons, 2018). We can see that a number of issues remain to be resolved with regard to the precise rela- tionship between female choice and male adornment. In contrast to this debate, there is, however, general consensus that males and females differ both physically and behaviourally due to the process of sexual selection. Recently sexual selection theory has become an important yet controversial tool for the study of human behaviour. We will return to this debate in Chapter 4. What’s So Good about Sex? In order for sexual selection to operate, clearly members of a species must engage in sex. Sexual reproduction is so common that we tend to take it for granted that this is the normal way of produc- ing offspring. But not all species use sex as a means of reproduction. Asexual reproduction is more common in the animal kingdom than people might think. Many unicellular organisms, for example, make clones of themselves by splitting into two; a process known as fission, and even among multi- cellular organisms, asexual reproduction is quite common (in which case it is called parthenogen- esis or ‘virgin birth’). In some multicellular species there may be both sexual and asexual periods during the life cycle, as is the case for aphids and water fleas, whereas for others parthenogenesis may be their only method of reproducing (in which case they are called obligate parthenogens). Examples of animals which are obligate parthenogens include certain species of fishes such as the Amazon molly and several species of whiptail lizard. To complicate matters further, in bees, 64 Sexual Selection wasps and ants (the hymenopteran social insects), male offspring develop from unfertilised eggs but females develop from fertilised ones. This means that the queen reproduces by both asexual and sexual means in the same season. Asexual reproduction is not, however, limited to insects and microscopic organisms; even among warm-blooded vertebrates such as domestic chickens, Chinese quail and turkeys, there are now well-documented cases of parthenogenesis on occasions (Crews, 1994; Parker and McDaniel, 2009). Why Bother with Sex? You might at this point be asking why so many species engage in asexual reproduction. But this is the wrong question to pose. As two of the world’s leading evolutionary experts, John Maynard Smith (1971) and George Williams (1975), have pointed out, there are at least three heavy costs associat- ed with sexual compared with asexual reproduction. First, there is ‘the cost of meiosis’ (Williams, 1975), which means that you throw half of your genes away with each offspring produced (see Chapter 2). Second, there is the cost of producing males, which means that, in contrast to females, most males do not reproduce at all (which means that many of your offspring will fail to provide you with grandchildren). And third, there is the cost of courtship and mating during which a great deal of time and energy is used up which might have been spent feeding or avoiding predators. When these costs of sex are fully appreciated asexual reproduction suddenly appears to have a lot going for it. The real question is, if birds do it, bees do it, even parthenogenic fleas do it, why don’t we all reproduce asexually? The fact that asexual and sexual reproduction are both possibilities in such a wide range of species, and yet so many multicellular species rely on sex, suggests sex must have some clear advan- tage. Given the cost of meiosis alone (the loss of half of our genes with each offspring produced) as Maynard Smith (1971) has pointed out, when in competition with asexual reproduction, sex should win out only if it doubles the number of offspring produced. Imagine two females in a population, one of which reproduces sexually and the other asexually. Each time the asexual individual produces an offspring it will be a clone and therefore will have 100 per cent of its mother’s genes. In contrast, each time the sexual female produces an offspring it will take, on average, 50 per cent of its genes from its mother and 50 per cent from its father. This means the sexually reproducing individual will have to produce twice as many offspring as the asexual one in order to pass on as many of its genes. Since this problem became apparent in the early 1970s evolutionary theorists have been struggling with the question ‘what’s so good about sex?’ The answer, like so many things in evolution, is not straightforward. As Maynard Smith has conceded ‘we have all the answers, we just can’t agree on them’ (pers. comm.). Box 3.3 Are Females Really ‘Coy’? Given the costs of sex are nearly always higher for females than for males, ever since Darwin, it has generally been assumed that, in the game of sex, the former are more likely to be ‘coy’ than the latter. Moreover, many evolutionists have argued that females are also more likely to gravitate towards monogamy than males. This view, however, has been challenged by Sarah Hrdy. As an experienced field primatologist Hrdy often observed female non-human primates seeking and  The Parasite Theory and Honest Signalling 65 Box 3.3 (cont.) initiating sexual behaviour. In common chimps, for example, a female in oestrus typically mates four times an hour and this may be with up to 13 different males (see Chapter 4). This sort of behaviour appears to run counter to the notion of coy, monogamy seeking females. Hrdy (2000), however, has pointed out that, even though the costs of reproduction are higher for females, they can also benefit from polyandrous mating since such behaviour leads to increasing genetic var- iability in their offspring. Hrdy has even argued that this helps to explain this behaviour across species including in human females (Hrdy, 2000; 2009). Figure 3.5 Female chimpanzee with infant – but who’s the father? Sarah Hrdy found female chimps regularly mate with several males to improve variability in their offspring. Ratchets, Raffles and Tangles Having explored the costs of sex we are now ready to ask the fundamental question – what is so good about sexual reproduction? Currently there are a number of theories that vie for our attention. Fisher himself advocated the influential idea that sexually reproducing populations would have an advantage in being able to evolve faster in a rapidly changing environment (Fisher, 1958). He argued that, by combining together genetic contributions from both parents, sexually reproducing individu- als should show more variability in their offspring than asexual ones that would have to rely on for- tuitous mutations to arrive. A sudden dramatic change in the climate, for example, would wipe out many more of the asexual individuals compared with the more varied sexual ones. A modification 66 Sexual Selection of Fisher’s faster evolution argument is Muller’s ratchet. This is the argument of Hermann Muller (1964) and states that each time a harmful mutation arises in an individual in an asexual population it will be passed on to all of its offspring. Like a ratchet that can only turn in one direction, each time a new harmful mutation occurs it is added to the population. With each new generation the number of these deleterious mutations accumulates. In sexual populations, however, on average only half of the offspring will inherit each parental mutation. If the mutation depresses an individual’s reproduc- tive success then it will eventually lose out to those individuals in the population that do not have it. This means that sex wins out because it helps to eliminate harmful mutations that would otherwise build up in the population. Both Fisher’s and Muller’s arguments look at the evolution of sex from the viewpoint of the group or population. As we saw in Chapter 2, however, evolutionists today consider natural se- lection as acting primarily at the level of the individual or even the gene. In 1975 George Williams, the champion of individual selection, proposed the raffle analogy to explain the advantages of sex. In this analogy having offspring is rather like having a number of raffle tickets which may or may not lead to the prize of surviving and reproducing in a given environment. Since sex leads to varia- tion then each offspring is like having a new ticket with a different number. By comparison asexual reproduction is like providing all of your offspring with the same number on each ticket; the chanc- es of winning will be greatly reduced if the environment should change. Williams’ raffle analogy leads to the prediction that sex will be more common in highly unpredictable environments such as in streams and at high altitudes and latitudes while asexual reproduction will be more common in more stable environments. A number of observations appear to support Williams. Sexually pro- duced aphids have wings which allow them to disperse, whereas asexually produced aphids which stay put do not. Clearly, if your offspring are going to travel then they are going to meet a variety of conditions and it may therefore pay you to provide them with greater variability. The raffle analogy makes intuitive sense. Unfortunately, intuition is not hard evidence. When Graham Bell of Montreal University tested the prediction that sex would be more common where the environment is unpredictable he found quite the opposite. Sex, he found, is more common when the environment is less changeable such as in the seas and at lower altitudes and latitudes (Bell, 1982). The Effects of the Living and the Physical Environments The problem with Williams’ theory may be that it relies too much on the predictability of the phys- ical or abiotic environment. Others have subsequently built their arguments around the living or biotic environment. When you begin to consider the effects of predators, of parasites and of other members of your species then Bell’s finding begins to make sense. Where abiotic conditions are predictable and less severe then they will be favourable to you. The problem is that they will also be favourable to other organisms. Under predictable conditions you will encounter the greatest com- petition from those closest to you, that is, other members of your own species. This means it may pay you to be a bit different. Hence sex is more common where physical conditions are favourable. Based on his findings Bell has developed his own theory to explain the existence of sex. He calls it the tangled bank theory after Darwin’s description in The Origin of Species of the competition that takes place between the myriad of organisms living in an overgrown embankment. If Bell’s theory is correct then, due to the competition that individuals within a species have with each other, we would expect to see continual change over a geological time scale. Unfortunately for Bell’s tangled bank theory, the fossil record does not support this prediction. Species tend to remain the same  The Parasite Theory and Honest Signalling 67 for hundreds of thousands of generations and then quite suddenly alter very rapidly (Eldridge and Gould, 1972; Maynard Smith, 1993). The Red Queen So where does this leave us? As we’ve seen with theories about sexual selection and even about why sex occurs at all, it seems that every time a new theory is put forward it is very quickly shot down. However, one of the exciting developments of recent years is that we may now be on the threshold of a general consensus, not only with regard to sex but also with regard to a number of other aspects of evolution. As with the theories about what choosy females are looking for in males, once again it’s all to do with parasites. This is the theory of the Red Queen and, although it was introduced by Leigh Van Valen back in 1973, it has only recently made a major impact on evolutionary theory with regard to behaviour. The Red Queen is based on the notion that parasites and hosts are in a continual evolutionary battle or arms race. Box 3.4 Alice and the Red Queen Leigh Van Valen named his Red Queen theory of why sexual reproduction initially arose and why it is maintained in so many species after a passage in Lewis Carroll’s Alice through the Looking Glass. At one point Alice meets the short-tempered Red Queen who constantly rushes around but never seems to get anywhere. When Alice is running around with the Red Queen but they don’t seem to be making any progress she remarks, ‘In our country … You’d generally get somewhere else – If you ran very fast for a long time as we’ve been doing’, the Red Queen replies, ‘A slow sort of country! … Now here, you see, it takes all the running you can do, just to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!’ The Red Queen theory suggests that evolutionary change on one side of the equation leads to counteract- ing change on the other side which in relative terms appears as a standstill. Due to their short lifespan and their enormous numbers, bacteria, viruses and other micro- bial parasites evolve much more rapidly than their hosts. According to the Red Queen theory, the host produces variable offspring in retaliation to parasites so that, by chance, some of them will have resistance. It is this variability that, by lending resistance to at least some of the offspring, gives sex the edge in the population. Since each side in the arms race reacts to changes in the opposition’s camp, then each ends up pretty much where it started off. Changes in the immune system of higher animals may even lead to circular warfare between host and parasite whereby a form of resistance, which may have been overcome in one generation, might re-emerge when the parasite has altered many generations later (see Chapter 12). This may help to explain why many species remain largely unchanged over very lengthy geological periods. As an armchair argument the Red Queen appears to stand up well, but does the empirical evidence substantiate it? Bell’s finding that sex is more common when the environment is more stable fits in well with the Red Queen but this also fits in well with his own preference that it is competition between macro-organisms that maintains sex in a population. The acid test of the Red 68 Sexual Selection Queen is that sex should be more common where parasite pressure is greatest. Since many species can reproduce either sexually or asexually a good test would be to determine which method is fa- voured by a species that can do either under varying degrees of parasite pressure. One study that fulfils these criteria perfectly was conducted in New Zealand by Curtis Lively. It involves water snails of the species Potamopyrgus antipodarum. These snails live in both stable lakes and highly variable streams and they are able to make use of both asexual and sexual reproduction. Both the tangled bank and the Red Queen hypotheses would predict that sex should be more common in sta- ble lakes whereas asex should be more common in the unpredictable streams. This of course makes it difficult to determine which hypothesis would be supported by finding sex more common in one environment over the other. Lively argued, however, that not only should sex be more common in the stable lake environment but so too would be the number of parasites. In strong support of the Red Queen, Lively (1987) discovered that in the lakes where rates of parasitism are high then sex is decidedly common, whereas in streams where parasitism is lower, asexual reproduction is more common. Lively and his co-workers have subsequently uncovered a similar finding with a small Mexican fish called a topminnow (Lively et al., 1990) and, more recently for a species of nematode (Morran et al., 2011). These findings lend clear support to the Red Queen and suggest that, although Bell may have been right to concentrate on biotic pressures as a driving force for sex, he may have been wrong about which biotic pressures. It’s not the big organisms that are most likely to kill you, it’s the ones you can’t even see. In relation to our own species, as Matt Ridley (1993) puts it: What killed your ancestors two centuries or more ago? Smallpox, tuberculosis, influenza, pneumonia, plague, scarlet fever, diarrhoea. Starvation or accidents may have weakened people, but infection killed them. (63) Currently the Red Queen is riding high. It may be that one of the most important consequences of the Red Queen lies beyond its effects on immunity from parasites – it lies in its effects on mate choice. Some evolutionists have argued that the Red Queen helps to explain why individuals of many spe- cies look for certain features in the opposite members of their population since these features are there to demonstrate a lack of parasites which might otherwise reduce reproductive potential. Sex, Evolution and Behaviour Armed with an understanding of the theories of natural and sexual selection we can now apply them to understanding behaviour. Understanding evolution as the differential survival of genotypes is quite easy when considering changes in morphological (physical) characteristics such as the number of eggs a hen lays or variability in, say, the length of a bird’s tail feathers. Understanding the relationship between evolution and behaviour is more difficult. Unlike a leg bone, behaviour does not fossilise and cannot be studied directly (Slater and Halliday, 1994; Rubenstein and Alcock, 2018). But if we consider an animal’s behavioural repertoire as a part of its phenotype then we can begin to see how it may also be shaped by evolution. Laying more eggs may help you to pass on more copies of your genes. Having longer tail feathers may help you to escape a bird of prey and, for males, may also attract females of your species to you. But having long tail feathers to enable you to escape a raptor or to attract a female would be useless if you were unable to recognise other animals as being dangerous or potential mates, respectively. Or to react appropriately to such stimuli. So, since behaviour has clear consequences for survival and for reproduction, genes which successfully modify an animal’s behavioural repertoire are passed on to its offspring.  The Parasite Theory and Honest Signalling 69 Of course, the consequences of an animal’s behaviour are always contingent on the environ- ment in which it lives. As we saw earlier we can break this environment down into abiotic and biotic components. Of the biotic components some will be potential food, some will be potential predators, some will be potential parasites but many will be members of your own species or conspecifics. Clearly, an animal’s behaviour helps it to solve the problems of its abiotic environment; if it’s too hot, cold, wet or dry it might be able to improve its immediate surroundings by digging a burrow and stay- ing put until things improve. But today, most experts agree that the biotic environment is of greater importance in shaping an animal’s behaviour (Drickamer et al., 2002). Of this living environment, it is becoming very clear that an animal’s conspecifics (or, strictly speaking, their ancestors) have been of the utmost importance in shaping the behavioural repertoire of a species (Rubenstein and Alcock, 2018). After all, it is other members of your species that you will need to cooperate or compete with. Cooperation is common among animal species; black-headed gulls band together to ‘mob’ larger carrion crows and drive them away from their nesting sites; African wild dogs form packs to bring down larger prey such as wildebeest (see Figure 3.6) and an individual ant could not survive without the combined and well-delineated efforts of its nestmates. But whereas cooperation is well documented in many species, competition is rife in all. Animals, in a sense, compete to become ancestors. Those individuals that successfully compete to pass on their genes to future generations become ancestors at the expense of others in the population. One of the most important elements of competition is competition for mates. In this way we can think of genes as biasing behaviour in ways that produce more copies of themselves. Clearly, genes that alter behavioural responses in ways that increase mating opportunities are likely to spread at the expense of genes that fail to do so. We can see that female choice and competition between males may both be very powerful forces in the evolution of behaviour. Figure 3.6 An African wild dog pack attacks a wildebeest. 70 Sexual Selection Box 3.5 Female Choice and Male Behaviour We saw earlier how male elephant seals attempt to mate with as many of the females that come ashore into their territories as they can. Some males are far more successful than others in this activity. In fact, one study showed that as few as 4 per cent of males are responsible for 85 per cent of the matings in a breeding season (Cox and Le Boeuf, 1977). Since males compete with each other for access to females, being bigger and more aggressive is clearly a successful adap- tive strategy for male elephant seals. Smaller and less aggressive males of previous generations were simply less successful; in this case it was the big bullies that left descendants. But what about the much smaller and less aggressive females? Is this one example where being much smaller than the males means that they really have no choice in the matter of repro- duction? It turns out that even in elephant seals, females are able to influence which male mates with them. When a bull mounts a cow seal she gives out a loud call that can be heard by nearby males. If the suitor is a subordinate male then he will invariably be chased off by a larger one who then takes his place. In this way females are able to ensure that the largest, most dominant males inseminate them. It might be argued that females in the past which did not give out such calls left fewer aggressive male descendants than those that did so. In this way we can see how female behaviour can have an effect on both the male and female offspring that are produced. And we can see that, even in cases where males are much larger than females, female choice plays a role in reproduction. Female Choice and Male Reproductive Success Females, arguably, exert an influence on the evolution of large size in male elephant seals and, as we saw earlier, female choice can lead to exaggeration of male features such as teeth and feathers. But is there any direct evidence of female choice affecting male reproductive success? Since the 1980s evidence has accumulated for the direct influence of female choice both on male physical features and on their reproductive success. Interestingly, the first clear-cut evidence of the importance of female choice involved precisely the feature that Fisher had suggested – elaboration of tail feathers (albeit not in peacocks). The African widowbird is a polygynous species (i.e. one male to sever- al females; see Chapter 4) that is found on the grassy plains of Kenya. In contrast to the mottled brown, short-tailed females, the jet-black male widow-birds have red epaulettes and, importantly, a very lengthy tail (on average 50 cm compared to the 7 cm average for females). Males maintain territories into which they attempt to attract females by sporadically leaping up above the long grass and showing off the magnificence of their fanned-out tail feathers. Females that land in a territory frequently mate with the resident male and afterwards build nests there into which they lay their eggs. It had long been suspected that females decide which territory to land in on the basis of the territory holder’s tail length, when Scandinavian ethologist Malte Andersson (1982; 1986) decided to check this with an elegant field manipulation. It involved the use of scissors and super-glue. Hav- ing determined the number of nests in a range of territories, by cutting and gluing their tail feathers he created four different groups of males. One group had their tails extended to 75 cm; another had their tails reduced to 14 cm and two control groups were allowed to retain their original tail length (see Figures 3.7 and 3.8). Following these manipulations, Andersson observed no change in the size  The Parasite Theory and Honest Signalling 71 Figure 3.7 Male African widowbird displaying tail. of male territories, but in contrast found that females now preferred to nest in the territories of the long- to the short-tailed males by a ratio of 4:1. Andersson’s field experiment has frequently been cited as the first real demonstration of the power of female choice as a driving force for male adornment and reproductive success but it has not been without its critics. For one thing female choice was inferred from the number of nests produced in a male’s territory rather than via the number of young fledged or from the number of matings observed. If Andersson’s study is open to interpretation, then a series of follow-up lab-based studies appear to demonstrate the effects of female choice unequivocally. Haines and Gould (1994), for example, demonstrated that female guppies preferred males with longer tails even though a longer tail slows them down (see Box 3.2). They discovered that when offered a choice between males of various sized tails, females chose both to spend more time with long-tailed males and to mate with them. Furthermore, the offspring produced also had longer tails just like their fathers. This finding is important because, as is the case for natural selection, for sexual selection to be accepted it is necessary that the features chosen are heritable. Incidentally, in what may be thought of as the icing on the cake for supporters of female choice, just as Fisher originally suggested, one study has now demonstrated that peahens really do prefer to mate with peacocks with the most elaborate tail feathers (Petrie et al., 1991; see Figure 3.9). Whether they do so because it demonstrates ‘good genes’ or simply because it is ‘sexy’ is still open to debate, however. Widowbirds, guppies and peacocks are just three examples from a literature that now abounds with such cases. In contrast to the ridicule that female choice was greeted with in the nine- teenth century, today it is seen as an increasingly important element in explaining the evolution of both male and female behaviour (Graves et al., 1985; Gould and Gould, 1997; Milan, 2010). 72 Sexual Selection Figure 3.8 Average number of nests in each (a) Before widowbird territory compared to male tail length. 2 Mean number of nests per male 1 0 (b) After 2 Mean number of nests per male 1 Ι ΙΙ 0 Shortened Elongated Controls Tail Treatment 8 Figure 3.9 Relationship between eye spots in a peacock’s train and his mating success. Number of mates 5 0 140 150 160 Number of Eye–Spots Competitive Males – and Female Behaviour If our ideas about the importance of female choice appear to have been strengthened in recent years we might also ask how well the other side of the argument stands up to scrutiny today. Do we still see males as the highly competitive sex? Throughout the animal kingdom it appears to be males that bluff and duel with each other. They appear to do so for resources such as territories or food, but  The Parasite Theory and Honest Signalling 73 ultimately all of the power struggles would be pointless without the presence of females. In the long run males compete for fertile females and they do so in many different ways. Lions, baboons and chimpanzees all form alliances in order to physically usurp other males and steal their mates (see Chapter 4). American red-winged blackbirds and European robins defend territories and sing to lure females into them. And many species of frogs and toads wrestle with each other for the opportunity to fertilise a female’s eggs even as she lays them. Box 3.6 Are You a Bit Neanderthal? A common put-down to someone we want to imply is both brutish and unattractive is to refer to them as ‘a Neanderthal’. Interestingly, despite this commonly held view of how primitive and unappealing the Neanderthals were, it now appears that there might be some science behind such a remark. The Neanderthals were a sub-species of early Homo sapiens – Homo sapiens neanderthalensis (although some experts consider them to constitute a separate species – Homo neanderthalensis; Humphrey and Stringer, 2018). In addition to a heavy, compact body they also had robust faces with large, wide noses and prominent brow ridges. Neanderthals (named after the Neander Valley in Germany where the first specimen was found) appeared around 130,000 years before present (YBP) in various parts of Europe and central Asia where they evolved from a different branch of Homo erectus (see Boxes 2.4 and 2.5). They disappeared from the fossil record around 25,000 YBP. Why they disappeared is uncertain. For some time it was assumed that anatomically modern Homo sapiens drove them to extinction. In recent years, however, it has been suggested that they may have interbred with anatomically modern Homo sapiens as some of their genes appear to have lived on and are with us today. In 2010 the Neanderthal Genome Project reported that modern humans living outside of sub-Saharan Africa typically have be- tween 1 and 4 per cent of Neanderthal genes (Green et al., 2010). More recently it has emerged that they coexisted with our direct ancestors for perhaps as long as 30,000 years and that there may have been quite extensive interbreeding during this period (Villanea and Schraiber, 2019). Such a finding suggests there may have been long-term, complex interactions occurring between these two sub-species between 55,000–25,000 YBP. This finding also raises the question: what role did sexual selection play here? Is it conceivable for early anatomically modern humans to have found some features of Neanderthals attractive? We can only speculate that at least some of our ancestors found at least some of them attractive enough to form a romantic attachment. One species which has been studied over many years in relation to male–male competition is the Scottish red deer (see Figure 3.10). By making field observations over a number of years, field ethologist Tim Clutton-Brock and his co-workers have demonstrated that the relationship between sexual selection and reproductive behaviour is more complex than had previously been thought (Clutton-Brock et al., 1982; Stopher et al., 2011). As is frequently the case for members of the deer family, stags live in all-male herds outside the breeding season. At the beginning of the breeding season, however, they begin to threaten each other and engage in physical combat in order to com- pete for harem territories. Harem territories are similar to resource defence harems except that the territory is the stable home of a core group of females while a series of males are displaced over the breeding season. Also, males frequently attempt to round up and steal females from nearby 74 Sexual Selection Figure 3.10 Red deer stags wrestling. territories. As with the elephant seals, males are much larger than their female counterparts, the does – about twice their size in fact. Additionally, males have much larger antlers. Stags that are suc- cessful in defending a harem must constantly be vigilant, however, since threats to their supremacy are common. Typically a stag will warn off challengers by producing some 3000 loud roars each day. When an intruding stag makes a challenge the two males undergo a highly ritualised sequence of responses. This begins with a long series of roars – if the intruder cannot keep up he will normally withdraw at this point. If he does not back down then the next stage is parallel walking during which each stag appears to eye up the size and strength of his competitor. If at this point neither backs down then the competitors lock their antlers and a vigorous wrestling match ensues until one of the combatants is exhausted and retreats. Due to their variability in size, in comparison to the does, red deer stags vary greatly in their reproductive success. Extensive field studies, however, have revealed that size can also pay dividends for females in the game of reproduction. Larger does are able to exclude smaller ones from the lushest parts of the territory and by improving their own grazing opportunities are able to increase the quantity of milk they provide for their suckling calves (Clutton-Brock et al., 1982). This means that the calves of a dominant doe are most likely to build up the fat reserves necessary to survive the first winter. Furthermore, the most important predictor of an adult stag’s reproductive success is his weight at the time of weaning. This means that the size and com- petitive behaviour of a doe plays a very important role in determining the success of her male offspring. This demonstrates how intrasexual selection can also be important to both sexes and that the female–female competition of one generation can have a knock-on effect on male–male competition in the next.  The Parasite Theory and Honest Signalling 75 Box 3.7 Why Are Some People Gay? The Paradox of Homosexuality In our role as university lecturers, we have both frequently been asked the question ‘how do evolutionary psychologists explain the existence of gay people?’ The implication of the question is clear. If homosexual people form same sex romantic relationships then they are less likely to produce offspring and, given both natural and sexual selection work through the production of surviving offspring, then does this not falsify the role of evolution in human mating behaviour? (The students may not have put it quite like this – but this is clearly where they are going!) It’s a fair question and one that some evolutionists have attempted to answer. Before exploring evolu- tionary explanations, let’s start with some terminology. The term homosexual has quite widely differing connotations in different cultures (as does the term ‘gay’) and is sometimes used as a noun or a verb. Using the term as a noun may be problematic in that people are much more than simply their sexual orientation. Hence, those who study the origins of sexual orientation gen- erally prefer to use the terms androphilia (man-loving) and gynephilia (women-loving) (Cart- wright, 2016; Vasey et al., 2020). This means that both men and women can be either androphilic or gynophilic. This also means that the question we need to explore is why are some women gynophilic and some men androphilic? One answer is to suggest that sexual orientation is free from biological/evolutionary influ- ence. The problem with this stance is that, at least in the case of male androphilia, there is strong evidence from twin studies it is influenced by genetic factors (Alanko et al., 2010). Moreover, the frequency of male androphilia (a little under 6 per cent) appears to be very similar regardless of socio-cultural factors (Vasey et al., 2020). Both of these findings suggest that, as a heritable trait, we need to consider how such forms of sexual orientation might arise within an evolution- ary context. Currently four evolutionary-based explanations have been proposed to explain male androphilia (note that few studies have considered female gynephilia) (Cartwright, 2016): kin selection models; sexually antagonistic selection; heterozygous advantage; fraternal birth order effects. We examine each in turn. The kin selection model can be traced back to E. O. Wilson who spec- ulated in 1975 that homosexual behaviour may be maintained in the population by kin selection. That is, individuals can pass on copies of their genes indirectly by adopting the role of, for ex- ample a supportive uncle or aunt (Wilson, 1975). To Wilson such individuals could be likened to sterile worker ants. Until recently, this speculation has not been well supported with most studies reporting equivocal findings for this hypothesis (Cartwright, 2016). Rahman and Hull (2005), for example, using a sample of 120 men from London found no difference between ‘gay’ and ‘straight’ men in self-reported levels of generosity towards kin. Recently, however, a team led by Canadian psychologist Paul Vasey has uncovered a degree of support for Wilson’s idea. In fact Vasey and his co-workers found quite strong evidence for the kin selection hypothesis in Samoa. In this country there are three recognised genders; male, female and the fa’afafine. The fa’afafine, who are transgender androphilic males (effeminate men who are attracted to other men), make large sacrifices for their nephews and nieces regularly guiding resources towards them (Vander- Laan and Vasey, 2012; Vasey et al., 2020). In fact taking on this avuncular role is considered to 76 Sexual Selection Box 3.7 (cont.) be the norm for the fa’afafine. Interestingly, Nila et al. (2018) have reported similar findings in Java in Indonesia, where androphilic men show elevated generosity to their nieces and nephews. Critics might argue that, despite these findings, this kin selection model does not have strong sup- port in Western societies – but Vasey and co-workers have suggested that Samoan and Indonesian societies may be closer to our common ancestral environment which might help to explain how this phenomenon arose in our species. Sexually antagonistic selection is the process whereby a gene or genes which enhance fit- ness when located in one sex, simultaneously reduce fitness when found in the other. In the case of male androphilia the prediction here is that female relatives of androphilic men who share the same X chromosome will have increased levels of fecundity. A number of studies appear to support this suggestion including Camperio-Ciani et al. (2004) who found that mothers of andro- philic men had an average of 2.7 babies whereas those of gynophilic men had an average of 2.3 babies. Moreover, this study also reported a higher rate of homosexual men on the mother’s side of the family than on the father’s side. This is supportive since the portion of the X chromosome would have to have come from the mother’s side for this model to work. Heterozygotic advantage can be used to explain why some alleles, which potentially reduce fitness in the homozygous genotype, can be maintained due to advantages conferred on relative who are heterozygous for those genes (see Chapter 2). Hence the existence of same sex attraction is presumed to be related to advantages conferred on relatives (as is also the case for kin selection and sexual antagonistic models). In this case the argument, which can be traced back to Hutchin- son in 1959, has become further developed by Edward Miller in the twenty-first century. Miller (2000) proposes that genes which confer same sex attraction are pleiotropic and lead, in many ‘straight’ men to an increase in sensitivity and empathy (both features attractive to women) in the heterozygous condition, but also to androphilia in homozygous men. This somewhat speculative hypothesis has some support from the finding that ‘straight’ men who are better able to identify with women are sexually more successful (Zietsch, 2008). Of course this finding is merely con- ducive with the hypothesis and by no means conclusive evidence. Finally, the fraternal birth order effects hypothesis is based on the finding that the further down birth order a male child is born the more likely they are to grow up to be androphilic (Blanchard, 2018). The suggestion here is that, when a family has a number of boys who are likely to produce grandchildren for you, then mechanisms exist which shunt latter born male siblings down the path to a ‘helpers-at-the-nest’ role (i.e. like older siblings who help to feed their younger siblings in some bird species). Note that this overlaps with the kin selection hypothesis to the point where it might even be seen as a variant of it. The strongest evidence for this hypothesis is simply the strength of the finding of a relationship between androphilia and being low down in the birth order (Blanchard, 2018). In summary with regard to answering our original student’s question we can make three quite confident assertions. First, most research has been conducted on why some men are an- drophilic rather than why some women are gynophilic. Second, currently experts have more theories than answers to explain the evolutionary conundrum of homosexuality. Third and finally, there is clearly a great deal of overlap between these hypotheses. Perhaps, as Vasey has recently commented, ‘the way forward in solving the evolutionary conundrum that is male androphilia will require viewing these alternative processes as complimentary [sic], rather than mutually exclusive’ (Vasey et al., 2020, 373).  Summary 77 Perhaps it is too simplistic to consider each sex in isolation when assessing the effects of sexual selection on a species. Perhaps in order to understand the strategy of one sex we must always consider the strategies of the other and the ecological pressures that exist. Furthermore, field studies that have considered sexual selection demonstrate how it not only affects body size and weaponry but also levels of aggression and the social structure of a group of animals. The more we look at sexual selection, the more intertwined and all pervading we realise it is. In Chapter 4 we come a little closer to home and consider the effects of sexual selection on mate choice in ourselves and our close relatives. Summary In 1871, in The Descent of Man, and Selection in Relation to Sex, Darwin introduced the notion of a new selective force – sexual selection. Sexual selection leads to features that help individu- als gain access to mates and takes two forms – intrasexual and intersexual selection. Intrasexual selection involves competition between members of one sex for access to the opposite sex, while intersexual selection involves members of one sex (usually males) attempting to attract members of the opposite sex. In nature these forces are believed to lead to elevated levels of aggression, greater body strength and the development of attractive features in males. For females, sexual selection leads to choosiness over mates. In 1930 Ronald Fisher suggested that ancestral females selected males with good features that aided survival such as long tail feathers. Once females had selected such features, over evolution- ary time, these features might become greatly exaggerated in males, since females are constantly choosing the most outstanding examples. These features might then become further exaggerated beyond their original function. Fisher called this ‘runaway selection’. Robert Trivers suggested that females should be choosy about whom they reproduce with. Be- cause they invest more in offspring than males, females have more to lose from making a bad choice. Males, on the other hand, lose very little if they make a bad decision and should therefore be less discriminating about sex. Trivers called the effort that each sex puts into producing off- spring ‘parental investment’. Due to gestation periods and nurturing activities such as suckling, the asymmetry in parental investment is greater in mammals than in other animals. Amotz Zahavi proposed that males develop elaborate features as impediments to demonstrate to females that they are able to survive despite having such a handicap – the ‘handicap hypothesis’. In contrast to Fisher and to Zahavi, Hamilton and Zuk suggested that male adornments have evolved to demonstrate to females their lack of parasites. Many animal species reproduce asexually. Single-celled organisms frequently reproduce through fission (splitting into two new individuals), and many multicellular organisms reproduce parthe- nogenically (development from an unfertilised egg). As Maynard Smith and Williams have both pointed out, sexual reproduction has a number of costs that asexual reproduction lacks. These include the cost of meiosis (i.e. losing half of your genes each time you reproduce), the cost of producing males (many of which will not reproduce) and the cost of courtship. The realisation that such costs exist has made sexual reproduction an area of debate among evolutionists. A number of theories have been proposed to explain the existence of sexual reproduction. Fisher suggested that, since there is greater variability in sexually produced offspring, sex speeds up 78 Sexual Selection evolution. Muller suggested that sex gets rid of harmful mutations which would otherwise build up in a population. Williams suggested the raffle analogy whereby variation in offspring is like having a number of different raffle tickets. Because future environmental pressures are difficult to predict, it pays individuals to provide their offspring with different raffle tickets (i.e. varia- tion). Bell proposed the tangled bank theory in which individuals have to vie with living (biotic) competitors rather than solving the problems of the non-living (abiotic) environment. Recently, however, attention has turned towards the Red Queen theory of sex as proposed by Van Valen. The Red Queen theory suggests that parasites and hosts are in a continual evolutionary arms race – the host produces variable offspring through sex so that, by chance, some of them will have resistance to pathogens. Behavioural patterns have both survival and reproductive value. Sexual selection theory and the notion of female choice have recently become important concepts for the understanding of be- haviour. There is now clear evidence from a number of species, such as birds, fishes and marine mammals, that female choice has been a driving force in the evolution of male adornment and aggressive behaviour. Because they produce fewer offspring, evolutionists have struggled to understand why some peo- ple form same sex romantic relationships. Currently four explanations have been suggested to explain this evolutionary conundrum: kin selection, whereby genes are passed on via generosity to non-descendant kin, sexually antagonistic selection whereby genes which enhance fitness in one sex, simultaneously reduce fitness in the other, heterozygous advantage whereby the homozy- gous condition is maintained in the population due to advantages afforded to their heterozygous relatives and finally, fraternal birth order, whereby latterborn individuals take on a ‘helpers-at-the- nest’ role. Questions 1. Some critics of evolutionary theory have suggested that the widespread existence of homosexual behaviour in both men and women means that human sexual behaviour is no longer related to in- clusive fitness theory. Consider the four proposed evolutionary explanations that have been devel- oped to explain this evolutionary conundrum. Do you feel that one or more of these explanations stands up to scrutiny? 2. Female American jacanas (a species of wading bird) are larger and more aggressive than their male counterparts. This is known as an example of ‘sex role reversal’ in the animal kingdom. Based on this very brief information, what predictions would you make about the reproductive behaviour of both males and females of this species? 3. Arguably many traits might have arisen from either natural or sexual selection. An example of this might be birdsong. How might we distinguish whether a bird’s song evolved via natural or sexual selection? 4. What’s so good about sex?  Further Reading 79 Further Reading Barkow, J. H. (1989). Darwin, Sex, and Status: Biological Approaches to Mind and Culture. Toronto: University of Toronto Press. Considers how sexual selection theory and knowledge of cultural practices can be combined to help us understand human sexuality. Also considers homosexual practices in Melanesia. Cronin, H. (1991). The Ant and the Peacock: Altruism and Sexual Selection from Darwin to Today. Cambridge: Cambridge University Press. Insightful and detailed history of the sexual selection debate. Milan, E. L. (2010). Looking for a Few Good Males: Female Choice in Evolutionary Biology. Baltimore: Johns Hopkins University Press. Presents a history of sexual selection in relation both to animal and to human behaviour. Prum, R. O. (2018). Evolution of Beauty: How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World. New York: Penguin Random House. Up-to-date account of how sexual selection affects mate choice in birds and humans. Vasey, P. L., Petterson, L. J., Semenyna, S. W., Gómez, F. R. and VanderLaan, D. P. (2020). Kin selection and the evolution of male androphilia. In L. Workman, W. Reader and J. H. Barkow (eds.). The Cambridge Handbook of Evolutionary Perspectives on Human Behavior (366–77). Cambridge: Cambridge University Press. Zuk, M. and Simmons, L. W. (2018). Sexual Selection: A Very Short Introduction. Oxford: Oxford University Press. Brief, but clearly drafted account of the current status of sexual selection written by two experts in the field.