The result of random mating that leads to a change in the genetic composition of a population.

12.3.1.2 Assortative Mating

Assortative mating is the tendency for people to choose mates who are more similar (positive) or dissimilar (negative) to themselves in phenotype characteristics than would be expected by chance. If these characteristics are genetically determined, positive assortative mating may increase homozygosity in the population. An important difference between inbreeding and positive assortative mating is that inbreeding affects all loci, while assortative mating affects only those that play a role in the phenotype characteristics that are similar. Clinical examples of positive assortative mating are those between individuals who are profoundly hearing impaired or blind, which in some cases may be attributable to the same genotypes.

Non-Random Mating and Population Structure

Non-random mating leads to departures from Hardy–Weinberg proportions. For example, inbreeding and positive assortative mating (where individuals prefer to mate with phenotypically similar individuals) yield an excess of homozygotes. By contrast, negative assortative mating (where opposites attract and individuals prefer to mate with phenotypically different individuals) results in excess of heterozygotes. Population structure also causes departures from Hardy–Weinberg proportions. For example, consider what happens when samples are drawn from multiple populations instead of a single randomly mating population. If these samples are pooled together and there are allele frequency differences between source populations the resulting mixture will have an excess of homozygotes. This reduction in heterozygosity is known as the Wahlund effect (Wahlund, 1928). In practice, departures from Hardy–Weinberg proportions due to non-random mating and population structure tend to be genome-wide (i.e., their effects can be seen at multiple loci).

Assortative Mating

Assortative mating is nonrandom mating based on phenotypes rather than between relatives. Positive-assortative mating or negative-assortative mating occurs if the mated pairs in a population are composed of individuals with the same phenotype more often, or less often, than expected by random mating, respectively. Positive-assortative mating is in some ways analogous to inbreeding in that similar phenotypes, which might have similar genotypes, are more likely to mate than random individuals from the population. Some types of assortative mating are also similar to inbreeding in that they do not change allele frequencies but do affect genotype frequencies. On the other hand, negative-assortative mating may result in balancing selection and the maintenance of genetic variation. Many assortative mating models do change allele frequencies because the proportion of individuals in the matings differs from the proportion in the population. An important point to remember is that assortative mating affects the genotype frequencies of only those loci involved in determining the phenotypes for mate selection (and genotypes at loci nonrandomly associated with those loci), whereas inbreeding affects all loci in the genome.

In a survey of assortative mating studies, Jiang et al. (2013) found that most of the examples of assortative mating were for positive-assortative mating. There appears to be positive-assortative mating for a number of traits in humans, such as height, skin color, and intelligence, although the consequent phenotypic correlation is often not very large. In addition, there also appears to be positive correlations among mates in humans that have particular phenotypes, such as deafness, blindness, or small stature. Of course, there are many different genetic (and nongenetic) causes for deafness, blindness, or small stature so that such a phenotypic correlation may not result in a genetic correlation (for deafness, see Nance and Kearsey, 2004). Rather strong positive-assortative mating may occur in plants when a pollinator forages at a given height or is attracted to a given flower color and, as a result, tends to pollinate plants similar to the ones where the pollen was collected. Similar effects may also occur when flowering time is variable, and only plants that flower simultaneously pollinate each other.

Jiang et al. (2013) found few examples of negative-assortative mating in their review. Some examples are, however, in some plants where successful fertilization occurs only between individuals with different flower types. Although less generally accepted, another example is in populations where rare males (or females) have a mating advantage over more common types. Some reports suggest that negative-assortative mating in mammals and other vertebrates may be based on major histocompatibility complex (MHC) differences.

The overall support for MHC-based, negative-assortative mate choice in humans is mixed and contentious. The most widely known example is the ‘t-shirt study’ in which female Swiss university students ranked the smell of t-shirts worn by male students on characteristics such as pleasantness (Wedekind et al., 1995). The findings of this study suggested that females preferred the odor of males that differed at MHC genes, except when they were on birth control pills, in which case they preferred males that were similar at MHC genes! Further, a follow-up study examining some of the same pairs found no correlation between the rankings for the two different studies.

Several recent studies have examined the correlation of mates for MHC in humans compared to the correlation of genes in the rest of the genome. The first such study found a small but significant (partly due to high statistical power) negative correlation in 30 couples at the MHC region of −0.043 compared to the average in the rest of genome of −0.00 016 (Chaix et al., 2008). However, this level of assortment appears small in a biological sense and nine other genomic regions had higher levels. Subsequently, Derti et al. (2010) concluded that the findings of Chaix et al. (2008) were not statistically robust and they found nonsignificant results in another small-sized, independent sample. These sample sizes appear much too small to draw inference about genomic assortative mating but a study underway of assortative mating in about 10 000 pairs using genome-wide SNP data (P. Visscher, personal communication) should give definitive estimates.

A striking example of negative-assortative mating is in wolves from Yellowstone National Park for gray and black coat color (Hedrick et al., 2016b). Black coat color in wolves is caused by a dominant allele at a beta-defensin gene. In the surveys of mating pairs at Yellowstone from 1995 to 2014, 166 out of 261 (64%) of the matings were between different color wolves, either gray males × black females or black males × gray females (Table 3) with a significant negative correlation of −0.27.

Table 3. The number of matings observed between gray and black wolves in Yellowstone National Park from 1995 to 2014 (Hedrick et al., 2016b)

4.2.3 Nondimensional Structure

There is extensive nonrandom mating among genetically distinct subpopulations of A. gambiae s.s.75 and possibly within A. coluzzii,82 known as chromosomal and/or molecular forms. The amount of gene flow among these populations and between species in Mali has been measured,83 and gene flow between forms seem internally consistent. However, the amount of hybridization varies considerably from location to location. Because some forms are more persistently present than others, and even absent at some locations, the amount of crossing will vary from place to place. But there are apparently intrinsic factors that also play a role in the degree of between-form hybridization.

Nondimensional Structure

There is extensive nonrandom mating among genetically distinct subpopulations of A. gambiae s.s., known as chromosomal and molecular forms (described later). Taylor et al. (2001) measured the amount of gene flow among these populations and between species in Mali in a variety of ways. Their measures of gene flow between forms in Mali seem internally consistent. However, the amount of hybridization between forms varies considerably from location to location. Because some forms are more persistently present than others, and even absent at some locations, the amount of crossing will vary from place to place. There are apparently intrinsic factors that also play a role in the degree of between-form hybridization.

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 MHC-dissimilar 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.

Disassortative Mating

Disassortative mating (sometimes called negative assortative mating) occurs when mates are chosen to be more phenotypically dissimilar than would arise by chance alone. Disassortative mating is not only the opposite of assortative mating in terms of the phenotypes displayed by mating pairs but also in its evolutionary and genetic consequences. This can be shown by the simple one-locus, two allele model of 100% disassortative mating given in Table 3.7. In this model, every genotype has a distinct phenotype and mates at random only with those individuals with a different phenotype, with no gender effects.

Table 3.7. A Model of 100% Disassortative Mating at a Single Locus With Two Alleles, A and a, With Each Genotype Having a Distinct Phenotype

SUM = GAA × GAa + GAA × Gaa + GAa × Gaa is used to standardize the mating frequencies so that they sum to 1.

As can be seen from Table 3.7, this system of mating produces many heterozygotes and few homozygotes—just the opposite of assortative mating. For example, suppose we started out with Hardy–Weinberg genotype frequencies with p = 0.25, with an initial heterozygote frequency of 0.375. Then in a single generation of disassortative mating as given by Table 3.7, the frequency of heterozygotes would increase to 0.565. Unlike the assortative mating model, in this case the allele frequency also changes from 0.25 to 0.326, so disassortative mating is a strong evolutionary force at the single locus level. However, with p = 0.326, the expected heterozygosity under random mating is 0.439, so there is still a heterozygous excess under disassortative mating with f = −0.286. Hence, disassortative mating resembles avoidance of inbreeding, but unlike avoidance of inbreeding, it only affects the loci contributing to the phenotype for which disassortative mating is occurring and loci in linkage disequilibrium with them. In addition, unlike avoidance of inbreeding, disassortative mating alters allele frequencies and tends to stabilize them at intermediate levels.

At the multi-locus level, disassortative mating can bring together into the same family alleles that have opposite effects on phenotypes. This could potentially generate some linkage disequilibrium, but by also causing excesses of heterozygosity, disassortative mating dissipates linkage disequilibrium much more rapidly than random mating (recall, recombination only changes gamete frequencies in double heterozygotes). Hence, disassortative mating is not as effective as assortative mating in generating or maintaining linkage disequilibrium.

A potential example of disassortative mating in humans is the major histocompatibility complex (MHC) (Laurent and Chaix, 2012a,b). MHC is a genomic region containing multiple genes coding for molecules whose role is to present self- and nonself-derived peptide antigens to T cells, thereby playing a critical role in immune response and in organ transplant success. MHC is a 3.6 megabase-pair long region located on the short arm of chromosome 6 in the human genome. Many of these same MHC genes influence body odor, and studies in other species and possibly humans indicate disassortative mating at MHC mediated by olfactory cues (Havlicek and Roberts, 2009). As expected for a region under disassortative mating, the MHC region shows a significantly higher level of heterozygosity than other regions of the human genome (Laurent and Chaix, 2012b). However, many studies do not indicate disassortative mating at MHC, and a metaanalysis of MHC effects on human mating revealed both MHC-dissimilar and MHC-similar matings in various studies (Winternitz et al., 2017). This seemingly contradictory pattern appears to be an artifact of population ethnic heterogeneity in observational studies that tend to indicate assortative mating versus experimental studies with more control over sociocultural biases that tend to indicate disassortative mating or mating for diverse MHC mates (Winternitz et al., 2017). In many areas of the world, human populations from diverse geographical areas and with different cultures have been brought together, as will be discussed in detail in Chapter 6. North America is one such area, and many of the studies on MHC have been performed on North American populations. Assortative mating by “ethnicity” has been historically quite strong and reduces genetic admixture among the descendants of these historic populations, although assortative mating by “ethnicity” has been diminishing with each successive generation (Sebro et al., 2017). Although “ethnicity” is not a genetic trait per se, it is often associated with some degree of genetic differentiation that reflects the historical origins of the parental populations that have been brought together into a single geographic region (Chapter 6). Hence, assortative mating in North America by “ethnicity” has resulted in deviations from Hardy–Weinberg and linkage disequilibrium for those loci that were differentiated between the parental population gene pools (Sebro et al., 2017), which includes the MHC cluster. When “ethnicity” and other sociocultural biases that influence mate choice are not controlled, it appears as if there is assortative mating for MHC, but when these factors are eliminated or controlled, it appears as if there is disassortative mating for MHC (Winternitz et al., 2017).

Hybridization and Mate-Choice Learning

Although mate-choice imprinting often results in positive assortative mating, typically with conspecifics, the potential exists for misimprinting, or imprinting on the wrong species. Hybridization between species of Darwin’s finches, for example, is known to occur and is thought to result from misimprinting. Additionally, crossfostering experiments conducted in the wild have demonstrated that some bird species will imprint on a foster parent of another species, resulting in heterospecific pairings.

Heterospecific matings could result in hybrid offspring and hybrid zones are not uncommon in nature. What role then, if any, does mate-choice imprinting play in hybrid zones? Using an artificial neural network, Brodin and Haas demonstrated that phenotypes of pure species are learned faster and better than those of hybrids, potentially leading to selection against hybrids. Further spatial simulations combined with empirical data on dispersal demonstrate that mate-choice imprinting can maintain a hybrid zone under natural conditions.

E POPULATION IDENTITY

The development of dialects between neighboring populations of potentially interbreeding individuals could lead to assortative mating; this in turn might benefit individuals if there are local genetic adaptations that can thereby persist. Nottebohm (e.g., 1972) suggested that dialects that are common in birds might have this effect. Although the idea has received some subsequent support, particularly in the white-crowned sparrow (Zonotrichia leucophrys, Baker and Cunningham, 1985), the weight of evidence is against it. For example, white-crown dialect boundaries do not seem to limit dispersal, song learning in males may occur after dispersal, and females often mate with males singing a different dialect from their natal one (see Catchpole and Slater, 1995, pp. 205–209 for a more detailed discussion). Even though this idea is now generally discounted in birds, it could still be true for marine mammals and bats that possess a similar potential for quick dispersal. If these animals return to their home area to mate, dialects might help to maintain local adaptations. Even in the relatively homogeneous marine environment, differences in local adaptations could exist between coastal and pelagic populations or between areas with different prey species.

In many of the examples of geographic variation in mammal calls the actual extent of each population is unknown. Even though some of the locations where seals have been found to differ in their vocalizations are several thousand kilometers apart, these species are mobile as well as widely distributed and could easily cover such distances in their migrations. Humpback whale populations in different oceans on the other hand may well be truly isolated and their dialects are therefore unlikely to be adaptive in maintaining population identity. Variations in call structure of different primate populations have been interpreted as possible evidence for vocal learning by several authors. If call variations between neighboring populations are actually learned, a function in population recognition might be a reason. However, there is no clear evidence for learned differences yet.

Assumptions of the Twin Method

Analytical requirements include the assumption of equal environments for twins-reared-together, as well as no assortative mating. The equal environments assumption (EEA) states that the shared environment (e.g., family environment, school environment) contributes equally to a trait in both MZ and DZ pairs. The vast majority of analyses which have tested for EEA violation across multiple psychological and psychiatric traits have indicated little support for EEA violation, thus providing sufficient confidence in the findings from studies of twins-reared-together, though it must be noted that some controversy remains over the adequacy of tests for violations of the EEA.

A second assumption is the absence of assortative mating – that is, spouses or mates do not select one another on the basis of the trait in question. There is ample evidence that spouses are moderately similar in terms of cognitive abilities, extant from the time of marriage. For aging-related cognitive traits (i.e., cognitive aging, AD), there are few data reported on spouse similarity. For now, it appears that the similarity between spouses for dementia is no greater than the similarity between any two people of the same age and sex.