Sexual Selection [M.Tevfik Dorak]

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SEXUAL SELECTION

M.Tevfik Dorak, M.D., Ph.D.

Current debate on Cooperative Games and Sexual Selection (PubMed - Science)

Sexual selection is selection for characters that enhance mating success. Darwin was impressed by the fact that qualities of sexual attractiveness were often the reverse of qualities leading to individual survival. He thought that gaining a higher chance to win mates was worth the risk conferred by such characters. Bright colours, long tails, plumes, antlers and horns threaten the survival of the animal but they also give them an advantage in fighting other males or attracting females. To Darwin, sexually selected characters were of no use other than being attractive to the females. He described sexual selection as selection in relation to sex. Wallace, however, thought that all those characters were more than ornaments with some utilitarian quality which females benefited for choosing. In his view, the ornamentations are used to advertise genuine quality as only the healthiest males can afford doing so; mating with them will generate more and healthier offspring.

Sexual selection leads to the evolution of characters that are apparently maladaptive. In view of the modern view of (inclusive) fitness, however, natural selection and sexual selection are not distinct and opposing processes. Superficially, sexual selection favours elaborate sexually dimorphic characters and natural selection opposes it because of their interference with survival. When fitness is seen as reproductive success rather than simply survival, sexual selection promotes morphological characters that would enhance reproductive success, thus, this is no different from what natural selection does. As long as the sexually selected characters do not prevent the individual attaining breeding age, sexual selection increases reproductive success of the individual whatever the overall survival cost is.

Sexual selection causes sexual dimorphism since it usually concerns males. This could lead to misidentification of individual specimens, particularly fossils. Natural selection in relation to sex may cause very rapid evolutionary change (runaway selection; see below). It may even lead to the formation of new species. It is also possible that sexual selection could have caused extinction of some species. The logic behind the fact that sexual selection mainly concerns males is simple. Males produce an enormous number of small sperms without investing too much energy, whereas, females produce a few large and nutritious eggs and they are very costly to them. If a male mates with several females, he increases the number of his progeny, but for females it makes no difference. A female gains only a little from having a large number of copulations with different males. Therefore, males in general are promiscuous but females are choosy because they want their few progeny to be of highest possible quality. There is also another reason. In species where females invest more in offspring, females will be the choosier sex. Females, then, want to increase the quality of their progeny by mating with particular males rather than others. All other things being equal, males are under strong selection to mate with as many females as possible. The selection forces on females act to be selective in terms of which males father their progeny. In summary, eggs represent a limited resource for which males must compete. There is usually a trade-off between mating behaviour and parental care.

Competition among males to obtain mates caused the evolution of intrasexual and intersexual selection. Pre-copulatory intrasexual selection (male-male competition) works through male aggression to claim the disputed females and intersexual selection (female choice) promoted the development of sexually attractive conspicuous characters but no fighting. In some mating systems male aggression and female choice for male characters are both involved (post-copulatory counterparts of these mechanisms are sperm competition and cryptic female choice, see below). Elephant seals are polygamous; pregnant females arrive on the breeding ground and gather together, giving birth in September; within three weeks they are ready for mating again. In October, a single male, which can be three times larger than the female, will claim a harem of as many as a hundred females, and will fight any other male that approaches his territory, proclaiming his ownership with a loud cry. Only fully mature males have the size and strength to keep such a harem. When a male approaches a female, the female cries and starts a fight among males to be copulated by the strongest of them (Le Boeuf BJ, 1972; Cox & Le Boeuf, Am Nat 1977;111(978):317-35). This is an example of sexual selection enticed by the females. A female elephant uses the same tactic to make sure she is mating with the strongest male in the group. Wood frogs (Rana sylvatica) exhibit explosive, synchronous breeding on a spring night. They gather in thousands at ponds where males compete intensively for females and even attempt to dislodge the amplexing male. Females also show choosiness by physically dislodging weakly amplexing males from their backs, therefore showing their preference for larger males. Red deer is another polygamous species in which a few dominant males mate with most of the females. It has to be noted that the harem masters among elephant seals and red deer have very much shorter reproductive lifespans than the females they defend. In elks, during rutting, the larger males are preferred by females through the correlation between the body size and pitch of the voice (the larger the body, the lower the pitch).

Sexual selection in species where females are heterogametic (e.g., having two different sex chromosomes 'ZW' such as birds, butterflies and moths) occurs mainly by the elaboration of ornate male secondary sexual characteristics, whereas in species where females are homogametic (e.g., having two copies of the same sex chromosome 'XX' such as mammals) sexual selection results predominantly in inter-male rivalry and the evolution of traits such as horns, antlers and large body size (all of which are testosterone-dependent). Another important factor determining the pressure of sexual selection is that males in monogamous species are subject to weaker sexual selection than males in polygynous species.

Since for biological reasons females are the choosy sex, it would be beneficial for them if there were some physical indicators of a quality of the genes of a male. Such externally visible clues to good genes would help them to make their choice. One such character would be the age of male since old age itself is a direct marker for survival ability. The selection of males with larger song repertoire by some birds may be due to the correlation of song repertoire with age. Other physical features used for selection by females may indeed be markers for male quality. A female Satin Bower Bird is, for example, attracted to a bower built by a male and is rich in rare blue objects. The males constantly fight and raid each other's bowers, so that a well-kept bower indicates the owner's superiority (Borgia G, 1985; see also Borgia Lab website).

There are three main theories currently being considered in the explanation of female choice [another grouping consists of the Fisherian run-away, viability indicator, sensory exploitation and antagonistic seduction models (Jennions & Petrie, 2000)]:

1. Run-away Selection Theory (RA Fisher, 1958): According to Fisher, if a majority of females prefer a particular kind of male, other females would be favoured if they mate with the same kind of males because their sons will be attractive to many females. Every individual will tend to inherit its mother’s genes for preferring its father, and its father’s genes for the qualities preferred. These two (groups of) genes will then segregate together and under certain circumstances, due to positive feedback, may lead to runaway selection of more and more exaggeration of the quality preferred. This would continue until the disadvantage, in terms of male survival, exceeds the reproductive advantage for males. Eventually, all the males in the population will end up with a tail length at the optimum point. When all males come to have the same trait, there would be no genetic advantage to a female in choosing one rather than the other. Because of this major problem with this theory, more elaborate forms of it have been developed.

2. 'Good Genes' Theories

a) Strategic Choice Handicap Theory (Zahavi A, J Theor Biol 1975 & 1977): This theory tries to explain the evolution of conspicuous characters from a different point of view. It suggests that the physical characters that are operational in sexual selection have evolved as handicaps to mark the stronger males who have survived despite the handicaps they bear. There are two kinds of handicaps: conditional or strategic choice handicaps reducing fitness (such as long tail) and revealing handicaps which confer no reduction in fitness (such as the bright colouring). The assumption that the tails of the peacock, birds of paradise and other birds, and the antlers of deer are 'handicaps' that these traits (when inherited by the offspring) will penalize them is not very convincing. The terms 'advertisements' or 'status symbols' may describe these traits better.

b) Revealing Signal Theory (Hamilton & Zuk, 1982): This theory proposes that only males resistant to parasites would be able to display conspicuous features -not necessarily costly to them- to attract females. Thus, the ornaments (such as long tails, inflated throat poaches or bright plumage) simply reveal the state of health without damaging it so they constitute revealing handicaps. Female choice for males with the best-developed sexual characters would result in offspring that are likely to inherit genetically-determined resistance to parasites from their father. This theory is in line with Wallace’s opinion about sexually selected characters and offers a possible solution to two serious problems in the theory of sexual selection: (1) choosing such a male is adaptive for females, (2) heritable genetic variation in male characters may be maintained despite the strong directional selection on these characters which should theoretically be short-lived. Since most parasites have shorter generation times than their hosts, the host has to adapt to new varieties constantly which would keep the selection going. Perhaps, as Wallace advocated, ornamentations are advertising genuine quality. The essence of the good genes theory is that an ornament can be sustained only by genuinely healthy males in good condition. Female sticklebacks, for example, use male coloration in mate choice and avoid parasitized males (Milinski & Bakker, 1990). A bright ruddy complexion in Uakari Monkeys signals good health and resistance to monkey malaria; pale faced ones are sickly and have no sex appeal. It has been shown that the offspring of peacocks with more elaborate trains enjoy improved growth and survival (Petrie M, 1994). Similarly, in male great tits (Parus major), heritable variation in a plumage is an indicator of viability (Norris K, 1993).

Recently, a set of data supporting the Hamilton & Zuk model was presented from the Molecular Population Biology Laboratory of Lund University (see also Dustin Penn's Work). Pheasants are polygynous and cocks defend a harem with several hens. There is a marked difference in plumage between the males and only the hen cares for the chicks. Spurs are one of the most variable ornaments of male pheasants and they found that males with longer spurs survived better than short spurred ones and this was not a by-product of male-male competition. This observation indicates that spur length reflects male quality and that females can use this trait to choose among potential fathers and pick up only those with good genetic traits to mate with in order to increase the quality of their young. They found that offspring from long spurred males had an increased survival. In a sample of 110 male pheasants, there was a significant difference in spur length between different MHC genotypes. The MHC exists in all vertebrate animals and is the genetic complex involved in immunocompetence and disease resistance. They also found fewer than expected MHC homozygous individuals and different survival of different MHC genotypes (von Schantz T et al, 1989, 1994, 1996). These are the first data that directly support the "good genes" hypothesis predicting that females discriminate among males on the basis of secondary sexual characters in order to pass on genes for disease resistance which will improve fitness in their offspring. The same Laboratory also reported that male song repertoire in great reed warblers correlates with post-fledging survival of offspring and, females choose (older) males with large song repertoires, resulting in extra-pair fertilizations with neighbouring males (Hasselquist D et al, 1996; see also Why Do Birds Sing?).

It is well established that in vertebrates testosterone has an immunosuppressive effect, and thus males have greater susceptibility to infections (including parasitic ones). Folstad & Karter (1992) suggested that males exhibiting well-developed secondary sexual ornaments, such as the comb on a rooster or antlers on a deer, might possess genes that offset the immunosuppression that often accompanies the production of testosterone-dependent ornaments. It follows that only males with immune systems robust enough to withstand the compromise associated with high levels of testosterone can maintain elaborate secondary sex characters. Females choosing to mate with such males then have offspring that inherit not only the attractiveness of their father, but his ability to resist pathogens while maintaining elaborate ornaments. This hypothesis also suggests that the ornaments are markers of good genes. Folstad and Karter refer to the ornament as an immunocompetence handicap. For example, male red jungle fowl (Gallus gallus) with larger combs have higher testosterone levels but fewer lymphocytes (less immunocompetent) than less-ornamented individuals, suggesting that maintenance of the ornament causes a compromise in immunocompetence (Zuk M et al. 1995). In this model, the good genes are proposed to be immune response genes and the same MHC genes fit into this model well. Recently, Dicthkoff et al (2001) have provided evidence for the role of the MHC in the development of antlers in white-tailed deer. They showed correlations between a heterozygous MHC genotype and antler development, body mass and testosterone levels. Thus, the MHC may be involved in sexual selection as the genetic origin of the 'good genes' affecting the development of secondary sexual characters and the quality of the immune response both in intra and intersexual competition.

3. Sensory Bias or Passive Attraction Theory (Parker GA, 1982): This is the simplest and a very convincing theory. It suggests that the sexually selected characters (such as loud sounds, bright plumage, long tails) are simply more conspicuous and more likely to attract the attention of a female from a distance than less intense signals. The evolution of such signals, therefore, may have nothing to do with handicaps or male quality. They may just be the result of selection on males to be noticed by females. Female Natterjack toads, for example, simply choose the louder male. This idea is consistent with a well-known phenomenon by ethologists that many animals respond to supernormal stimuli: bigger, louder, and faster. Females who choose males with conspicuous, easy to recognize signals denoting which species they belong to, mate successfully with little cost. This easy choice behaviour would be favoured, even if the female gains no additional advantage through the attractiveness of her sons (Fisher's theory) or genetically high quality children of both sexes (good genes theories). Such easy choice signals of males may simply be enabling females to find a mate with minimal cost.

The overall conclusion is that although sexual selection is widely referred to in the literature as if it were a process distinct from natural selection, it should be regarded -as Darwin did- as a form of natural selection. Sexual selection is not some extra force in opposition to natural selection. It is about selection in relation to sex which is governed by the same processes involved in the evolution of characters that are not related to sex. It is basically natural selection acting differently on the two sexes.

The less appreciated form of sexual selection that has gained popularity lately is the cryptic female choice. This is a postcopulatory process of sperm selection probably for the genetically most divergent ones (another inbreeding avoidance mechanism). The selection for sperm may start as early as in the vagina, may involve the process called sperm capacitation in the uterus and the long journey of the sperm along the reproductive tract. Finally, the ovum itself may have mechanisms to distinguish between sperms. The overall effect is selective fertilization. This is particularly important in animals where forced copulations (as in yellow dung fly, reptiles and ducks) or extra-matings (as in zebra finch, mice) take place. Cryptic female choice forms the post-copulatory continuation of female mate choice whereas sperm competition is the continuation of male-to-male competition. Cryptic female choice consists of many other mechanisms including selective abortion. Pre-copulatory sexual selection results in non-random mating and post-copulatory selection in selective fertilization/implantation/abortion. Most interestingly, similar mechanisms also exist in plants: pollen competition/selection, differential pollen tube growth, selective fertilization, selective fruit and seed abortion.

The above-mentioned (pre-copulatory) female enticed sexual selection in seals has its correspondent in post-copulatory phase of selection. Female feral fowl prefer dominant males but if they are sexually coerced by subordinate males and their manipulation of dominant males fails, they differentially eject the sperm from subdominant males (Pizzari & Birkhead, 2000). This example shows that sexual selection continues after copulation and post-copulatory mechanisms exist to fix the mistakes made in earlier phases. In fact, pre-copulatory mechanisms may not even exist for several reasons (males cannot reliably signal their quality or females cannot detect signals). In these situations, females are only left with the post-copulatory mechanisms they can use. By mating polyandrously, sexual selection occurs in copula (Jennions & Petrie, 2000). Post-copulatory mechanisms of female choice may be more successful at detecting genetic compatibility because males cannot disguise their identity as easily (Zeh & Zeh, 1997; Newcomer et al, 1999). Genetic compatibility is detected via signals on sperm, and sperm-soma or egg-sperm interactions but avoidance of genetic incompatibility is not the only benefit of post-copulatory sexual selection (Evans & Magurran, 2000).

Sexual selection and speciation: Sexual selection affects the process of mating and the slightest change to the process of mating, if it prevents interbreeding, means a new species exists (via reproductive isolation mechanisms).

Evidence for sexual selection: Preference of prominently collared males of the Guppy (Poecilia reticulata) by females correlates with the presence of more collared male fish (Houde & Endler, 1990). The number of colourful fish is high when there is not much predation (sexual selection), but low when there are predators in the habitat (natural selection). Colour patterns of natural populations of guppies are, therefore, a compromise between sexual selection and predation avoidance. They are relatively more conspicuous to guppies at the times and places of courtship and relatively less conspicuous at the times and places of maximum predator risk (Endler JA 1991).

The great crested newt provides an example of a correlation between a sexually selected character and general condition. Newts with higher crests during breeding time are in better conditions. Therefore, selection of males in terms of their crest height is selection for healthy ones.

The male fiddler crab E.albus has one greatly enlarged claw with which he displays to females; the female fiddler crabs mate preferentially with males with larger claws. In this case this exaggerated male character is positively advantageous in survival terms as it provides enhanced protection against predation by birds.

In seaweed flies, the male character preferred by females is the adult size. The adult size has large additive genetic variance in males, but not in females. The benefit of this selection is that virtually all the variance in male size is attributable to a chromosomal inversion system which is also a major determinant of larval viability, and male size is a reliable indicator of offspring survival for females (Wilcockson RW et al, 1995).

Courtship behaviour

Courtship behaviour widely varies among species. Cream-like hawk moth's courtship behaviour consists of aphrodisiac pheromones, love songs and aerobatic flights. Firefly uses light to attract mates. Fairy tern courtship begins with the male's flying around the female offering her a mackerel. During the courtship, males keep offering females more fish as gifts. Probably most bizarre behaviour during courtship is the one observed in mantis. The female chops off the male's head during copulation and a result of this, copulation continues more effectively as the brain has an inhibiting effect on male's sexual performance.

Mating systems

A. Monogamy: mating occurs with one mate only. 90% of birds are monogamous. This is because their young require parental care (see below).

B. Polygamy: mating occurs with many mates

1. polygyny: a male mates with several females, occurs especially when males have the control of resources or females. Creates strong selection for larger and stronger males (elephant seals).

2. polyandry: a female mates with several males. This is a very rare mating system. It occurs when suitable breeding sites are scarce and nests are subject to heavy predation (American Jacana or Lilly trotter).

Mating system is determined by several factors

1. Quantity of resources: rich environments tend to favour polygyny, impoverished environments monogamy.

2. Distribution of resources: patchy distribution of resources favours polygyny.

3. Predation: monogamy is favoured as a couple would better defend their territory.

4. Other determinants of social behaviour: living in groups may alter reproductive behaviour.

5. Female availability in time: synchronous breeding among females tends to favour polygyny.

6. Requirements of the young: depending on the development level of the newborn and the level of care it would require, males may be monogamous or polygynous.

In many species, females mate with more than one male as an insurance in case the first male is infertile. Multiple paternity also offers opportunities to increase the genetic diversity and the survival rate of the offspring. A general rule is that the smaller the proportion of males that mate, the more intense will be the selection for larger male size (10% in elephant seals, hence the huge size).

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