Genetics And Mate Choice Research Paper

1. Avoidance Of Inbreeding

Consanguinity is an important criterion of mate choice. Throughout the vertebrate, invertebrate, and plant kingdoms, the propensity to inbreed (mate with a blood relative) varies widely (Thornhill 1993). Some species of hermaphroditic plants mate predominantly with themselves—the seed is fertilized by pollen from the same individual. In others, mechanisms such as self-incompatibility have evolved to prevent self-fertilization. Hence, self-fertilization is not the unavoidable consequence of female and male functions occupying the same body. In species where the two sexes are separate, nuclear family incest—matings between father and daughter, mother and son, or full sibs (brother and sister with the same mother and father)—is the most extreme form of inbreeding. For some insects, mother–son and brother–sister matings are routine.

On the other hand, close inbreeding is unusual in birds and mammals. Of special interest are the nonhuman primates, where nuclear family incest, in particular, is rarely observed. Adult males of the chimpanzee, our closest relative, have seldom been seen mating with their mothers. Most, but not all, females refuse the sexual advances of males in their natal group old enough to be their fathers. The incidence of copulations between inferred maternal ( possibly full) sibs is low (Pusey 1980). However, matings between paternal half sibs may not be uncommon in the gorilla.

The claim is often made that behavioral mechanisms have evolved in birds and mammals to prevent close inbreeding. However, avoidance of incest is not necessarily based on recognition of family members. Because of a sex difference in dispersal, sons and daughters may not encounter their opposite-sex sibs or parents as adults. In the black-tailed prairie dog, for example, daughters usually remain in their natal area whereas the sons emigrate. Fathers may also leave or be evicted before their daughters mature. Under these circumstances, incest may be prevented even when matings are indiscriminate. The reason for such a dispersal pattern is unknown, but avoidance of inbreeding is a possible explanation. It is perhaps surprising, then, that the incidence of close inbreeding, mostly between half sibs, does not differ from the number expected if matings were occurring at random in the study area (Hoogland 1992).

Nevertheless, kin recognition has been implicated in some field studies and demonstrated in the laboratory. A likely mechanism is ‘sexual imprinting,’ the phenomenon in which sexual preferences expressed later in life are acquired through exposure at a very young age to other individuals, usually parents or sibs. A prairie dog female, for example, is less likely to come into estrus when her father is still present. Similarly, an older female of the medium ground finch mates with a male who sings a song differing from her father’s. Since song is culturally transmitted from father to son in this species, close kin are apparently recognized and avoided (Grant and Grant 1996). Finally, Japanese quail reared with sibs choose the company of first cousins over that of either sibs, third cousins, or unrelated individuals. Bateson (1982) infers from this experiment that quails learn the characteristics of close kin and subsequently develop a preference for mates differing somewhat from familiar individuals.

It is interesting that cousin marriage, which is a comparatively mild form of inbreeding, is highly popular in some human societies. In particular, in south India and in many Muslim populations, the incidence of first-cousin marriages exceeds 30 percent (Bittles 1994). The reasons for this preference are likely different from those operative in quails.

In contrast to cousin marriage which exhibits much regional variation in incidence, nuclear family incest, marital and nonmarital, has been prohibited and usually avoided in almost all human societies past and present that we know about. A well-known counter example comes from Roman Egypt, where one-sixth of all marriages among commoners were between full sibs (Bagnall and Frier 1994). The evidence comprises over 300 census returns preserved on papyri, from which pedigrees have been reconstructed. Although this example is certainly the exception rather than the rule, it cautions against naive explanations for the existence of incest taboos.

Westermarck (1891) proposed that ‘there is an innate aversion to sexual intercourse between persons living closely together from early youth.’ In particular, full sibs reared together are expected to avoid mating with one another, but not full sibs reared apart. Avoidance is also predicted when unrelated boys and girls are reared together in the same household. Thus, studies on the Chinese custom of sim-pua and on marriage patterns among Israelis reared together as children in kibbutzim seem to support the ‘Westermarck hypothesis.’ For example, the sim-pua is a girl who is adopted, often as an infant, into a family with a young boy, to be his future bride (‘little daughter-in-law’). After being brought up as sister and brother, they are forced to marry. Compared to other arranged marriages, the fertility of this type of marriage (minor marriage) is low, and the divorce rate is high (Wolf 1995).

This result is usually regarded as reflecting sexual dissatisfaction and supporting the Westermarck hypothesis. Nevertheless, marriages between foster sibs were in fact consummated. Moreover, in the case of institutionalized sib marriage in Roman Egypt, any aversion that may have existed was overridden. Hence, even if negative sexual imprinting occurs, it is apparently not sufficient to prevent an incestuous mate choice when other cultural pressures intervene.

If behavioral mechanisms such as sexual imprinting and sex-biased dispersal have evolved by natural selection to prevent close inbreeding in birds and mammals, there must be a selective disadvantage to mating with close kin. Sexual imprinting and sex-biased dispersal are assumed to be genetically determined capacities—hence innate. An inbred (born of related parents) offspring is known to have lower fitness than an outbred (born of unrelated parents) one. The decrease in fitness, normalized by the fitness of the outbred offspring, is called the inbreeding depression, and is estimated in practice by comparing survival to some arbitrary age. Inbreeding depression is believed to be caused by homozygosity for (having two copies of ) deleterious recessive genes. The more closely inbred an individual is, the more severe the inbreeding depression is expected to be.

Estimates of the inbreeding depression associated with nuclear family incest average 33 percent for 38 species of mammals in captivity (Ralls et al. 1988). In humans, one study with good controls obtained an estimate of 29 percent, although this estimate is inflated by the inclusion of morbidity (Adams and Neel 1967).

The conditions under which avoidance of inbreeding will evolve are difficult to compute, but some theory, mostly heuristic, exists for full-sib matings (Maynard Smith 1980). If all males have the same number of mates, then sib mating is selected against, and avoidance will evolve. This would be true of a strictly monogamous species. However, if the inbreeding depression is less than one-third, and a female by being incestuous can give her brother one extra mating, then it will be in her interests to do so.

Another factor that may offset the natural selection against incestuous matings is ‘reproductive compensation’—if offspring lost due to inbreeding depression are replaced. Similarly, if ecological or economic conditions are such that sibs can mate earlier than unrelated individuals, then lifetime reproductive success may be comparable—or even greater—for the incestuous pair. Keller and Arcese (1998) argue that this may be the reason why song sparrows do not purposefully avoid close inbreeding. In fact, the incidence of full-sib and parent–offspring matings was as expected if song sparrows were mating indiscriminately.

In modern human societies, age at marriage is lower when the spouses are cousins—and generally when related—than when they are unrelated. Perhaps because of this, or because of reproductive compensation, cousin marriages enjoy a higher fertility (live births) than nonconsanguineous unions (Bittles 1994). When on-going marriages in Roman Egypt are broken down by age, there is a relatively higher incidence of brother–sister and other close-kin marriages among the younger couples. Therefore, it is possible that sibs were marrying earlier than unrelated couples. Moreover, one of the most fertile couples are sibs, with eight surviving children (Bagnall and Frier 1994). If sib mating permitted an early start in reproduction during much of human evolutionary history, then sib mating rather than its avoidance may have been favored by natural selection.

2. Preference For A Mate Differing At The Major Histocompatibility Complex

In (positive) assortative mating, psychologically, behaviorally, or physically similar individuals pair up. Negative assortative, or disassortative, mating occurs as a result of attraction between dissimilar individuals. An example of positive marital assortment is the tendency of deaf persons to marry one another. Another example is the high correlation between the intelligence quotients of spouses. In the latter example, however, it is not known whether someone with an IQ comparable to one’s own is actually preferred as a marriage partner. Rather, people who marry one another have often experienced similar environments as children, and since the environment is a major determinant of IQ, spouses may incidentally have similar IQs.

Recently, Wedekind et al. (1995) suggested that humans prefer a mate differing at the major histocompatibility complex (MHC). MHC is an essential part of the vertebrate immune system. It comprises many genes, each of which is highly variable and exists in many alternative forms called alleles. In the human, the genes are called HLA-A, HLA-B, HLA-C, etc. (HLA human leucocyte antigen.) For illustrative purposes, let us focus on the HLA-A gene and assume that four alleles are present, which will be called A1, A2, A3, and A4. The pair of alleles in an individual defines the genotype of that individual. The genotypes could be A1A1, A2A2, A3A3, or A4A4, which are called homozygotes, or A1A2, A1A3, A1A4, A2A3, A2A4, or A3A4, which are called heterozygotes.

Mates can share two alleles (as when the genotypes of husband and wife are A1A2 and A1A2), one allele (A1A2 and A2A3, for example), or no alleles (A1A3 and A2A4, say). The hypothesis of disassortative mating asserts that sexual attraction is negatively correlated with the number of alleles shared. Hence, an individual of genotype A1A1, say, given a choice of three different partners whose genotypes are A2A2, A1A2, and A1A1, say, is predicted—all other things being equal—to prefer the first (A1A1 and A2A2 share no alleles) over the second (A1A1 and A1A2 share one allele) over the third (A1A1 and A1A1 share two alleles).

Theoretically speaking, disassortative mating for MHC may make evolutionary sense. Yamazaki et al. (1976) argue as follows. Heterozygotes for MHC genes have a higher fitness than homozygotes, because the presence of two alleles rather than just one would permit an immunological response to a wider range of antigens. Although the genotype that an individual is born with cannot be altered, the genotype of offspring is under some personal control. Namely, by choosing an MHC-dissimilar partner, the chances are improved that offspring will be heterozygotes. A second reason why disassortative mating for MHC might be favored by natural selection is that it leads to avoidance of inbreeding.

A preference for MHC-dissimilar mates is fairly well established in house mice. There is good evidence, at least in mice, that this preference is mediated by body odor, which is influenced by the MHC genes. More precisely, mice imprint on the MHC identities of the individuals by, or with, whom they are raised, who under normal circumstances would be extended family. They subsequently choose a mate differing in MHC from these individuals. Since, close relatives are on average more similar for their MHC than unrelated individuals, the resulting preference would be for MHC-dissimilar mates.

The human evidence is of two kinds. First, in a provocative experiment, male subjects were asked to each wear a T-shirt, and female subjects to rate the odors of these T-shirts for pleasantness (sexiness). The subjects, all of whom were students at a Swiss university, were also typed for their HLA-A, HLA-B, and HLA-DR genes. It turned out that the females preferred the odors of T-shirts worn by MHCdissimilar males to those worn by MHC-similar males (Wedekind et al. 1995).

Second, a direct test of whether humans mate disassortatively for MHC should be possible by typing married couples. To date, such an analysis has been done on the Hutterites (a North American reproductive isolate of European ancestry), South American Indians from the lower Amazon basin, and the Japanese. Only among the Hutterites has dissortative mating been demonstrated (Ober et al. 1997). In the other two populations, mating is apparently random with regard to MHC.

It is not clear why such contradictory results have emerged. One possibility is that, since the preference for MHC-dissimilar mates is weak, it may sometimes be overwhelmed by other biological or cultural factors. In particular, a preference for cousin marriages will mask any tendency towards disassortative mating. However, there is no evidence of cousin marriages among the couples sampled in the above mentioned studies.

3. Genetically Fixed Preferences S. Acquired Preferences

In all of the above examples, mating preferences are apparently acquired by sexual imprinting. Despite the title of this research paper, convincing demonstrations of genetically fixed preferences are hard to find. Even in insects, appropriate social behavior is often contingent on learning to distinguish different categories of individuals—nestmates from intruders, for example.

Nevertheless, a possible example of a genetically fixed preference occurs in ladybird beetles. Ladybirds are polymorphic for color and markings, and females show a preference for melanic males. Majerus et al. (1982) subjected this preference to artificial selection by permitting only those females who mated with melanic males to lay eggs. When the experiment was continued for four generations, a substantial increase in the level of preference was observed.

Cultural transmission of preferences is also difficult to prove. Surprisingly, the best evidence comes not from humans, but rather from small tropical fish— guppies, sailfin mollies, and three-spined sticklebacks—where the phenomenon is known as ‘matechoice copying’ (Dugatkin 1992). Mate-choice copying is said to occur when a female is more likely to choose a specific male after observing another female doing so. The following three-phase experiment is conducted to demonstrate mate-choice copying.

In phase one, a female (focal female) is given a choice of two males. If the focal female shows a consistent preference for one of these males, then in phase two, a second female (model female) is placed near the nonpreferred male in view of the focal female. Finally, in phase three, the model female is removed, and the focal female is again given a choice of the two males. Mate-choice copying is implied, if the focal female’s preference is reversed as a result of seeing the model female and the nonpreferred male together. (It is not clear how long the reversal of preference is maintained.)

The experiment must control for confounding effects. For example, the focal female might be attracted by the nonpreferred male’s activity during or after his interaction with the model female, rather than by the presence of the model female. Or the focal female may simply be exhibiting a tendency to join other females, as is apparently the case with fallow deer. White and Galef (1999), who investigated matechoice copying in Japanese quail, point out other complications in the interpretation of such experiments.

Given this emphasis on socially learned sexual preferences in fish and birds, it is perhaps ironic that most research on humans—by the evolutionary psychologists—has attempted to identify preferences that are relatively impervious to social influence. For example, it is claimed that men are attracted to women with a low waist-to-hip ratio (WHR)—an hourglass figure. This appears to be true in several Westernized cultures. Moreover, since women with lower WHR are apparently more fecund (physiologically able to give birth) (Zaadstra et al. 1993), Singh (1993) argues that it is adaptive for a man to have such a preference, whence it has evolved to become a panhuman— culturally invariant—male characteristic. The logic is fine, but the prediction has yet to be verified. Recently, Yu and Shepard (1998) studied WHR preferences in an isolated Peruvian population unexposed to Western media. Contrary to prediction, an overweight woman with a high WHR was most attractive and desirable as a spouse for the men of this population.

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