Major histocompatibility complex and sexual selection

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MHC sexual selection has been observed in the black-throated blue warbler. Black-Throated Blue Warbler.jpg
MHC sexual selection has been observed in the black-throated blue warbler.

The major histocompatibility complex in sexual selection concerns how major histocompatibility complex (MHC) molecules allow for immune system surveillance of the population of protein molecules in a host's cells. In 1976, Yamazaki et al. demonstrated a sexual selection mate choice by male mice for females of a different MHC[ clarify ].

Contents

Major histocompatibility complex genes, which control the immune response and effective resistance against pathogens, have been able to maintain an extremely high level of allelic diversity throughout time and throughout different populations. Studies suggest that the MHC is involved in mate choice for many vertebrates through olfactory cues. There are several proposed hypotheses that address how MHC-associated mating preferences could be adaptive and how an unusually large amount of allelic diversity has been maintained in the MHC. [1] [2]

The vast source of genetic variation affecting an organism's fitness stems from the co-evolutionary arms race between hosts and parasites. There are two nonmutually exclusive hypotheses for explaining this. One is that there is selection for the maintenance of a highly diverse set of MHC genes if MHC heterozygotes are more resistant to parasites than homozygotes—this is called heterozygote advantage . The second is that there is selection that undergoes a frequency-dependent cycle—and is called the Red Queen hypothesis .

Hypotheses

In the first hypothesis, if individuals heterozygous at the MHC are more resistant to parasites than those that are homozygous, then it is beneficial for females to choose mates with MHC genes different from their own, and would result in MHC-heterozygous offspring—this is known as disassortative mating. The hypothesis states that individuals with a heterozygous MHC would be capable of recognizing a wider range of pathogens and therefore of inciting a specific immune response against a greater number of pathogens—thus having an immunity advantage. Unfortunately, the MHC-heterozygote advantage hypothesis has not been adequately tested. [2] A non-MHC immune genes across species exhibit heterozygote disadvantage, or no advantage. [3] [4] [5] [6] [7] [8] In mice, increased MHC heterozygosity reduces fitness, challenging this hypothesis. MHC-heterozygous females had significantly reduced fitness compared to homozygotes. [9] This finding has been replicated in another study in mice and again in fish [10] [11] In some cases, excess heterozygosity can lead to decreased fitness. [12]

The optimality hypothesis states too much variability in the MHC can result in a failure of T-cells to distinguish themselves non-selves, and thereby increase the risk of autoimmune disease. This would confer greater fitness to individuals without a large degree MHC diversity. [6] [13] Autoimmune diseases are associated with MHC loci. In humans, those with greater MHC diversity have a greater risk for autoimmune disorders. MHC diversity may be low "because foreign peptides have to stand out against the self-background." On an individual level, MHC diversity tends to be low. Across many species, there is intermediate heterozygosity in the MHC. Overall evidence supports intermediate MHC heterozygosity is best. [14]

The Red Queen hypothesis asserts that MHC diversity is maintained by parasites. If individuals' MHC alleles render different resistances to a particular parasite, then the allele with the highest resistance is favored, selected for, and consequently spread throughout the population. Recombination and mutation cause generation of new variants among offspring, which may facilitate a quick response to rapidly evolving parasites or pathogens with much shorter generation times. However, if this particular allele becomes common, selection pressure on parasites to avoid recognition by this common allele increases. An advantageous characteristic that allows a parasite to escape recognition spreads, and causes selection against what was formerly a resistant allele. This enables the parasite to escape this cycle of frequency-dependent selection, and such a cycle eventually leads to a co-evolutionary arms race that may support the maintenance of MHC diversity. This hypothesis has empirical support. [15] [2] [16]

Parasites are in a constant arms race with their host: harvestman suffering from mite pest Parasitismus.jpg
Parasites are in a constant arms race with their host: harvestman suffering from mite pest

The inbreeding avoidance hypothesis has less to do with host-parasite relationships than does the heterozygote advantage hypothesis or the Red Queen hypothesis. The extreme diversity in the MHC would cause individuals sharing MHC alleles to be more likely to be related. As a result, one function of MHC-disassortative mating would be to avoid mating with family members and any harmful genetic consequences that could occur as a result. The hypothesis states that inbreeding increases the amount of overall homozygosity—not just locally in the MHC, so an increase in genetic homozygosity may be accompanied not only by the expression of recessive diseases and mutations, but by the loss of any potential heterozygote advantage as well. [17] [2] Animals only rarely avoid inbreeding. [18] The inbreeding avoidance hypothesis has been "ruled out as an explanation for the observed pattern of MHC-dependent mate preference" because relatedness is not associated with mate choice. [19]

In the course of searching for potential mates, it would benefit females to be able to discriminate against "bad" genes in order to increase the health and viability of their offspring. If female mate choice occurs for "good" genes, then it is implied that genetic variation exists among males. Furthermore, one would presume that said difference in genes would impart a difference in fitness as well, which could potentially be chosen or selected for.

Generally, the extreme polymorphism of MHC genes is selected for by host-parasite arms races (the Red Queen hypothesis); however, disassortative mate choice may maintain genetic diversity in some species. Depending on how parasites alter selection on MHC alleles, MHC-dependent mate-choice may increase the fitness of the offspring by enhancing its immunity, as mentioned earlier. If this is the case, either through the heterozygote advantage hypothesis or the Red Queen hypothesis, then selection also favors mating practices that are MHC-dependent.

The exaggerated, elongated upper tail coverts make up the "train" of the peacock. Paonroue.JPG
The exaggerated, elongated upper tail coverts make up the "train" of the peacock.

Therefore, mate choice—with respect to the MHC—has probably evolved so that females choose males either based on diverse genes (heterozygote advantage and inbreeding avoidance hypotheses) or "good" genes. The fact that females choose is naturally selected, as it would be an advantageous trait for females to be able to choose a male that provided either an indirect or direct benefit. As a result of female choice, sexual selection is imposed on males. This is evidenced by genetic "advertisement"—an example of this would be the existence of exaggerated traits, such as the elaborate tail-feathers of male peacocks. However, in humans, both sexes exert mate choice.

The relationship between olfaction and MHC

MHC-based sexual selection is known to involve olfactory mechanisms in such vertebrate taxa as fish, mice, humans, primates, birds, and reptiles. [1] At its simplest level, humans have long been acquainted with the sense of olfaction for its use in determining the pleasantness or the unpleasantness of one's resources, food, etc. At a deeper level, it has been predicted that olfaction serves to personally identify individuals based upon the genes of the MHC. [20]

Human olfactory system. 1: Olfactory bulb 2: Mitral cells 3: Bone 4: Nasal epithelium 5: Glomerulus (olfaction) 6: Olfactory receptor cells Olfactory system.svg
Human olfactory system. 1: Olfactory bulb 2: Mitral cells 3: Bone 4: Nasal epithelium 5: Glomerulus (olfaction) 6: Olfactory receptor cells

Chemosensation, which is one of the most primitive senses, has evolved into a specialized sensory system. Humans can not only detect, but also assess, and respond to environmental (chemical) olfactory cues—especially those used to evoke behavioral and sexual responses from other individuals, also known as pheromones. Pheromones function to communicate one's species, sex, and perhaps most importantly one's genetic identity. The genes of the MHC provide the basis from which a set of unique olfactory coding develops. [20]

Although it is not known exactly how MHC-specific odors are recognized, it is currently believed that proteins bound to the peptide-binding groove of the MHC may produce the odorant. Each MHC protein binds to a specific peptide sequence, yielding a set of uniquely bound peptide-MHC complexes for each individual. During cellular turnover, the MHC-peptide complex is shed from the cell surface and the fragments are dispensed in bodily fluids such as blood serum, saliva, and urine. Scientists believe that commensal microflora, microorganisms that line epithelial surfaces open to the external environment such as the gastrointestinal tract and vagina, further degrade these fragments, which are made volatile by this process. Recently, it has been shown that receptors in the vomeronasal organ of mice are activated by peptides having similar characteristics to MHC proteins; further studies may hopefully soon clarify the exact transformation between MHC genotype and an olfactory mechanism. [1] [20] [21]

Empirical evidence

In humans

MHC similarity in humans has been studied in three broad ways: odor, facial attractiveness, and actual mate choice. [22] Studies of odor find MHC-dissimilarity preferences but vary in details, while facial attractiveness favors MHC-similarity and actual mating studies are varied. [22]

Specific studies

Several studies suggest that MHC-related odor preferences and mate choice are demonstrated by humans. However, the role of MHC in human mate choice has been relatively controversial. One study conducted by Ober et al. examined HLA types from 400 couples in the Hutterite community and found dramatically fewer HLA matches between husbands and wives than expected when considering the social structure of their community. [23] On the other hand, there was no evidence of MHC-based mate choice in the same study of 200 couples from South Amerindian tribes. [23]

Other studies have approached mate choice based on odor preference. In one study done by Wedekind et al., women were asked to smell male axillary odors collected on T-shirts worn by different males. Women that were ovulating rated the odors of MHC-dissimilar men as more pleasant than those of the MHC-similar men. Furthermore, odors of MHC-dissimilar men often reminded women of current or former partners, suggesting that odor—specifically odor for MHC-dissimilarity—plays a role in mate choice. [24]

In another study done by Wedekind et al., 121 women and men were asked to rank the pleasantness of the odors of sweaty T-shirts. Upon smelling the shirts, it was found that men and women who were reminded of their own mate or ex-mate had dramatically fewer MHC alleles in common with the wearer than would be expected by chance. If the selection for shirts was not random, and actually selected for MHC-dissimilar alleles, this suggests that MHC genetic composition does influence mate choice. Furthermore, when the degree of similarity between the wearer and the smeller was statistically accounted for, there was no longer a significant influence of MHC on odor preference. The results show that MHC similarity or dissimilarity certainly plays a role in mate choice. Specifically, MHC-disassortative mate choice and less similar MHC combinations are selected for. [25] One interesting aspect of the Wedekind's experiment was that in contrast to normally cycling women, women taking oral contraceptives preferred odors of MHC-similar men. This would suggest that the pill may interfere with the adaptive preference for dissimilarity. [24] [25]

In primates

There is evidence of MHC-associated mate choice in other primates. In the grey mouse lemur Microcebus murinus , post-copulatory mate-choice is associated with genetic constitution. Fathers are more MHC-dissimilar from the mother than are randomly tested males. Fathers have more differences in amino acid and microsatellite diversity than did randomly tested males. It is hypothesized that this is caused by female cryptic choice. [26]

In other animals

In mice, both males and females choose MHC-dissimilar partners. Mice develop the ability to identify family members during early growth and are known to avoid inbreeding with kin, which would support the MHC-mediated mate choice hypothesis for inbreeding avoidance. [2]

Fish are another group of vertebrates shown to display MHC-associated mate choice. Scientists tested the Atlantic salmon, Salmo salar , by observing effects of MHC upon natural spawning salmon that resided in the river versus artificial crosses that were carried out in hatcheries. Logically, the artificial crosses would be bereft of the benefits of mate choice that would naturally be available. The results showed that the offspring of the artificially bred salmon were more infected with parasites: almost four times more than the naturally-spawned offspring were. In addition, wild offspring were more MHC-heterozygous than the artificially-bred offspring. These results support the Heterozygous Advantage hypothesis of sexual selection for MHC-dissimilar mate choice. [27] In another fish, the three-spined stickleback, it has been shown that females desire MHC diversity in their offspring, which affects their mate choice. [28]

Female Savannah sparrows, Passerculus sandwichensis, chose MHC-dissimilar males to mate with. Females are more likely to engage in extra-pair relationships if paired with MHC-similar mates and more dissimilar mates are available. Similarly, MHC diversity in house sparrows, Passer domesticus, suggests that MHC-disassortative mate choice occurs. [2]

MHC-mediated mate choice has been shown to exist in Swedish sand lizards, Lacerta agilis . Females preferred to associate with odor samples obtained from males more distantly related at the MHC I loci. [29]

Even though many species are socially monogamous, females can accept or actively seek mating outside of the relationship; [30] extra-pair paternity is a mating pattern known to be affiliated with MHC-associated mate choice. Birds are one of the more commonly studied groups of animals to exhibit this sexual behavior. In the scarlet rosefinch Carpocus erythrinus , females engaged in extra-pair paternity much less frequently when their mates were MHC-heterozygous. [31] In the Seychelles warbler Acrocephalus sechellensis , there was no evidence of MHC variation between social mates. However, when females' social mates were MHC-similar, they were more likely to participate in extra-pair paternity; in most cases, the extra-pair male was significantly more MHC-dissimilar than the social mate. [32]

MHC-mediated mate choice may occur after copulation, at the gametic level, through sperm competition or female cryptic choice. The Atlantic salmon, Salmo salar, is one species in which sperm competition is influenced by the variation in the major histocompatibility complex, specifically that of the Class I alleles. Atlantic salmon males have higher rates of successful fertilization when competing for eggs from females genetically similar at the class I genes of the MHC. [33]

Another species that exhibits MHC-associated cryptic choice is the Arctic charr Salvelinus alpinus . In this case, however, it seems that sperm selection is more dependent on the ovum. MHC-heterozygous males were found to have significantly more fertilization success than MHC-homozygous males; sperm count, motility, and swimming velocity were not shown to significantly co-vary with similarity or dissimilarity at the MHC. It is proposed that there is a chemo-attraction system responsible for the egg itself being able to discriminate and selectively choose between MHC-heterozygous and MHC-homozygous males. [34]

Contrary to the Atlantic salmon and the Arctic char, red junglefowl Gallus gallus males instead of females exert cryptic preference. Male junglefowl showed no preference when simultaneously presented with both an MHC-dissimilar and an MHC-similar female. However, they did show a cryptic preference by allocating more sperm to the more MHC-dissimilar of the two. [35]

Male sand lizards Lacerta agilis behave similarly to the male junglefowl. Initial copulation between a male and a female without any rivals was shown to be extended when the male sensed a higher female fecundity. However, second males adjusted the duration of their copulation depending on the relatedness between the female and the first male, believed to be determined by the MHC-odor of the copulatory plug. A closer genetic relatedness between a male and a female sand lizard increased the chances for a successful fertilization and rate of paternity for the second male. [36]

Abortional selection may be a form of cryptic female choice. Many studies on humans and rodents have found that females may spontaneously abort pregnancies in which the offspring is too MHC-similar.[ citation needed ] In addition, in vitro fertilizations are more likely to fail when couples have similar MHC genes.[ citation needed ]

MHC and sexual conflict

If males attempt to thwart female mate choice by mating with a female against her will, sexual conflict may interfere with the choice for compatibility at the MHC genes.

In Chinook salmon Oncorhyncus tshawytscha, females act more aggressively towards MHC-similar males than MHC-dissimilar males, suggesting the presence of female mate choice. Furthermore, males directed aggression at MHC-similar females. This was accompanied by male harassment of unreceptive females; however, there was a positive correlation between male aggression and reproductive success. The ability of the males to over-power the females' original mate choice resulted in the offspring of the targets of male aggression having low genetic diversity. Offspring with high genetic diversity seemed to happen only when the operational sex ratio was female-biased, when females were more likely to be able to exert mate choice, and males were less likely to harass females. These results suggest that sexual conflict may interfere with female mate choice for 'good' MHC genes. [37]

See also

Related Research Articles

<span class="mw-page-title-main">Inbreeding</span> Reproduction by closely related organisms

Inbreeding is the production of offspring from the mating or breeding of individuals or organisms that are closely related genetically. By analogy, the term is used in human reproduction, but more commonly refers to the genetic disorders and other consequences that may arise from expression of deleterious recessive traits resulting from incestuous sexual relationships and consanguinity. Animals avoid incest only rarely.

<span class="mw-page-title-main">Major histocompatibility complex</span> Cell surface proteins, part of the acquired immune system

The major histocompatibility complex (MHC) is a large locus on vertebrate DNA containing a set of closely linked polymorphic genes that code for cell surface proteins essential for the adaptive immune system. These cell surface proteins are called MHC molecules.

<span class="mw-page-title-main">Human leukocyte antigen</span> Genes on human chromosome 6

The human leukocyte antigen (HLA) system or complex is a complex of genes on chromosome 6 in humans which encode cell-surface proteins responsible for regulation of the immune system. The HLA system is also known as the human version of the major histocompatibility complex (MHC) found in many animals.

Disassortative mating is a mating pattern in which individuals with dissimilar phenotypes mate with one another more frequently than would be expected under random mating. Disassortative mating reduces the mean genetic similarities within the population and produces a greater number of heterozygotes. The pattern is character specific, but does not affect allele frequencies. This nonrandom mating pattern will result in deviation from the Hardy-Weinberg principle.

Heterosis, hybrid vigor, or outbreeding enhancement is the improved or increased function of any biological quality in a hybrid offspring. An offspring is heterotic if its traits are enhanced as a result of mixing the genetic contributions of its parents. The heterotic offspring often has traits that are more than the simple addition of the parents' traits, and can be explained by Mendelian or non-Mendelian inheritance. Typical heterotic/hybrid traits of interest in agriculture are higher yield, quicker maturity, stability, drought tolerance etc.

A heterozygote advantage describes the case in which the heterozygous genotype has a higher relative fitness than either the homozygous dominant or homozygous recessive genotype. Loci exhibiting heterozygote advantage are a small minority of loci. The specific case of heterozygote advantage due to a single locus is known as overdominance. Overdominance is a rare condition in genetics where the phenotype of the heterozygote lies outside of the phenotypical range of both homozygote parents, and heterozygous individuals have a higher fitness than homozygous individuals.

<span class="mw-page-title-main">Overdominance</span>

Overdominance is a rare condition in genetics where the phenotype of the heterozygote lies outside the phenotypical range of both homozygous parents. Overdominance can also be described as heterozygote advantage regulated by a single genomic locus, wherein heterozygous individuals have a higher fitness than homozygous individuals. However, not all cases of the heterozygote advantage are considered overdominance, as they may be regulated by multiple genomic regions. Overdominance has been hypothesized as an underlying cause for heterosis.

<span class="mw-page-title-main">Molecular ecology</span> Field of evolutionary biology

Molecular ecology is a field of evolutionary biology that is concerned with applying molecular population genetics, molecular phylogenetics, and more recently genomics to traditional ecological questions. It is virtually synonymous with the field of "Ecological Genetics" as pioneered by Theodosius Dobzhansky, E. B. Ford, Godfrey M. Hewitt, and others. These fields are united in their attempt to study genetic-based questions "out in the field" as opposed to the laboratory. Molecular ecology is related to the field of conservation genetics.

<span class="mw-page-title-main">Mate choice</span> One of the primary mechanisms under which evolution can occur

Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior. In other words, before an animal engages with a potential mate, they first evaluate various aspects of that mate which are indicative of quality—such as the resources or phenotypes they have—and evaluate whether or not those particular trait(s) are somehow beneficial to them. The evaluation will then incur a response of some sort.

<span class="mw-page-title-main">Lek paradox</span>

The lek paradox is the conundrum of how additive or beneficial genetic variation is maintained in lek mating species in the face of consistent sexual selection based on female preferences. While many studies have attempted to explain how the lek paradox fits into Darwinian theory, the paradox remains. Persistent female choice for particular male trait values should erode genetic diversity in male traits and thereby remove the benefits of choice, yet choice persists. This paradox can be somewhat alleviated by the occurrence of mutations introducing potential differences, as well as the possibility that traits of interest have more or less favorable recessive alleles.

Claus Wedekind is a Swiss biological researcher notable for his 1995 study that determined a major histocompatibility complex (MHC) dependent mate preference in humans.

<span class="mw-page-title-main">Odor</span> Volatile chemical compounds perceived by the sense of smell

An odor or odour is caused by one or more volatilized chemical compounds that are generally found in low concentrations that humans and many animals can perceive via their sense of smell. An odor is also called a "smell" or a "scent", which can refer to either a pleasant or an unpleasant odor.

Genetic matchmaking is the idea of matching couples for romantic relationships based on their biological compatibility. The initial idea was conceptualized by Claus Wedekind through his "sweaty t-shirt" experiment. Males were asked to wear T-shirts for two consecutive nights, and then females were asked to smell the T-shirts and rate the body odors for attractiveness. Human body odor has been associated with the human leukocyte antigens (HLA) genomic region. They discovered that females were attracted to men who had dissimilar HLA alleles from them. Furthermore, these females reported that the body odors of HLA-dissimilar males reminded them of their current partners or ex-partners providing further evidence of biological compatibility.

Host–parasite coevolution is a special case of coevolution, where a host and a parasite continually adapt to each other. This can create an evolutionary arms race between them. A more benign possibility is of an evolutionary trade-off between transmission and virulence in the parasite, as if it kills its host too quickly, the parasite will not be able to reproduce either. Another theory, the Red Queen hypothesis, proposes that since both host and parasite have to keep on evolving to keep up with each other, and since sexual reproduction continually creates new combinations of genes, parasitism favours sexual reproduction in the host.

Odour is sensory stimulation of the olfactory membrane of the nose by a group of molecules. Certain body odours are connected to human sexual attraction. Humans can make use of body odour subconsciously to identify whether a potential mate will pass on favourable traits to their offspring. Body odour may provide significant cues about the genetic quality, health and reproductive success of a potential mate.

Inbreeding avoidance, or the inbreeding avoidance hypothesis, is a concept in evolutionary biology that refers to the prevention of the deleterious effects of inbreeding. Animals only rarely exhibit inbreeding avoidance. The inbreeding avoidance hypothesis posits that certain mechanisms develop within a species, or within a given population of a species, as a result of assortative mating and natural and sexual selection, in order to prevent breeding among related individuals. Although inbreeding may impose certain evolutionary costs, inbreeding avoidance, which limits the number of potential mates for a given individual, can inflict opportunity costs. Therefore, a balance exists between inbreeding and inbreeding avoidance. This balance determines whether inbreeding mechanisms develop and the specific nature of such mechanisms.

The ovulatory shift hypothesis holds that women experience evolutionarily adaptive changes in subconscious thoughts and behaviors related to mating during different parts of the ovulatory cycle. It suggests that what women want, in terms of men, changes throughout the menstrual cycle. Two meta-analyses published in 2014 reached opposing conclusions on whether the existing evidence was robust enough to support the prediction that women's mate preferences change across the cycle. A newer 2018 review does not show women changing the type of men they desire at different times in their fertility cycle.

Mating choice in humans, as with human sexuality more generally, is a complex behavioural process involving biological, psychological, cultural and social elements. Its complexity is reflective of similar behaviours exhibited by other great apes where mating choices and sexual behaviours vary significantly not just between species but also within different populations of the same species.

Genetic incompatibility describes the process by which mating yields offspring that are nonviable, prone to disease, or genetically defective in some way. In nature, animals can ill afford to devote costly resources for little or no reward, ergo, mating strategies have evolved to allow females to choose or otherwise determine mates which are more likely to result in viable offspring.

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