Mate choice

Origins and history

Charles Darwin first expressed his ideas on sexual selection and mate choice in his book The Descent of Man, and Selection in Relation to Sex in 1871. He was perplexed by the elaborate ornamentation that males of some species have, because such features appeared to be detrimental to survival and to have negative consequences for reproductive success. Darwin proposed two explanations for the existence of such traits: these traits are useful in male-male combat or they are preferred by females. This article focuses on the latter. Darwin treated natural selection and sexual selection as two different topics, although in the 1930s biologists defined sexual selection as being a part of natural selection.

In 1915, Ronald Fisher wrote a paper on the evolution of female preference and secondary sexual characteristics. Fifteen years later, he expanded this theory in a book called The Genetical Theory of Natural Selection. There he described a scenario where feedback between mate preference and a trait results in elaborate characters such as the long tail of the male peacock (see Fisherian runaway).

In 1948, using Drosophila as a model, Angus John Bateman presented experimental evidence that male reproductive success is limited by the number of mates obtained, while female reproductive success is limited by the number of pregnancies that she can have in her lifetime. Thus a female must be selective when choosing a mate because the quality of her offspring depends on it. Males must fight, in the form of intra-sexual competition, for the opportunity to mate because not all males will be chosen by females. This became known as Bateman's principle, and although this was a major finding that added to the work of Darwin and Fisher, it was overlooked until George C. Williams emphasised its importance in the 1960s and 1970s.

In 1972, soon after Williams' revival of the subject, Robert L. Trivers presented his parental investment theory. Trivers defined parental investment as any investment made by the parent that benefits his or her current offspring at the cost of investment in future offspring. These investments include the costs of producing gametes as well as any other care or efforts that parents provide after birth or hatching. Reformulating Bateman's ideas, Trivers argued that the sex which exhibits less parental investment (not necessarily the male) will have to compete for mating opportunities with the sex that invests more. The differences in levels of parental investment create the condition that favours mating biases.

Direct and indirect benefits

Being choosy (having a bias in the context of mating) must incur a fitness advantage in order for this behaviour to evolve. Two types of fitness benefits (direct and indirect) are thought to drive the evolutionary mechanisms of mate choice:

Mechanisms

Currently, there are five mechanisms that explain the evolution of mate choice:

Direct and/or indirect benefits are driving the mating biases described in each mechanism. It is possible that these mechanisms co-occur although the relative roles of each have not been evaluated adequately.

Direct phenotypic benefits

Choosy individuals receive direct benefits from their mates and this results in immediate increased fecundity, or the number of offspring produced. If the competitive sex displays an ornamental trait that reliably indicates some direct benefit then strong selection will favor mating bias. Having a mating preference is advantageous in this situation because it directly affects reproductive fitness. Direct benefits are widespread and the evidence for this mechanism of evolution is well supported in empirical studies.

One example of a sexually selected trait with direct benefits is the bright plumage of the northern cardinal, a common backyard bird in the eastern United States. Male northern cardinals have conspicuous red feathers while the females are more cryptic in coloration. In this example, the females are the choosy sex and will use male plumage brightness as a signal when picking a mate because males with brighter plumage have been shown to feed their young more frequently than males with duller plumage. This increased help caring for the young lifts some of the burden from the mother so that she can raise more offspring than she could without help.

In the great reed warbler, females tend to be attracted to males with longer song repertoires since they tend to sire offspring with improved viability. In doing so, they gain indirect benefits for their own young. In the Utetheisa ornatrix, females select males based on body size, systemic content of pyrrolizidine alkaloid, and glandular content of hydroxydanaidal. As a result, these females demonstrate direct and indirect phenotypic benefits: they have offspring that are less vulnerable to predation because of their increased size and higher alkaloid content, increasing viability and fitness.

Sensory bias

The sensory bias hypothesis states that the preference for a trait evolves in a non-mating context and is then exploited by one sex in order to obtain more mating opportunities. The competitive sex evolves traits that exploit a pre-existing bias that the choosy sex already possesses. This mechanism is thought to explain remarkable trait differences in closely related species because it produces a divergence in signaling systems which leads to reproductive isolation.

Sensory bias has been demonstrated in guppies, freshwater fish from Trinidad and Tobago. In this mating system, female guppies prefer to mate with males with more orange body coloration. However, outside of a mating context, both sexes prefer animate orange objects which suggests that preference originally evolved in another context, like foraging. Orange fruits are a rare treat that fall into streams where the guppies live. The ability to find these fruits quickly is an adaptive quality that has evolved outside of a mating context. Sometime after the affinity for orange objects arose, male guppies exploited this preference by incorporating large orange spots to attract females.

Another example of sensory exploitation is in the water mite Neumania papillator, an ambush predator which hunts copepods (small crustaceans) passing by in the water column. When hunting, N. papillator adopts a characteristic stance termed the 'net stance' - their first four legs are held out into the water column, with their four hind legs resting on aquatic vegetation; this allows them to detect vibrational stimuli produced by swimming prey and use this to orient towards and clutch at prey. During courtship, males actively search for females - if a male finds a female, he slowly circles around the female whilst trembling his first and second leg near her. Male leg trembling causes females (who were in the 'net stance') to orient towards often clutch the male. This did not damage the male or deter further courtship; the male then deposited spermatophores and began to vigorously fan and jerk his fourth pair of legs over the spermatophore, generating a current of water that passed over the spermatophores and towards the female. Sperm packet uptake by the female would sometimes follow. Heather Proctor hypothesised that the vibrations trembling male legs made were done to mimic the vibrations that females detect from swimming prey - this would trigger the female prey-detection responses causing females to orient and then clutch at males, mediating courtship. If this was true and males were exploiting female predation responses, then hungry females should be more receptive to male trembling - Proctor found that unfed captive females did orient and clutch at males significantly more than fed captive females did, consistent with the sensory exploitation hypothesis.

Other examples for the sensory bias mechanism include traits in auklets, wolf spiders, and manakins. Further experimental work is required to reach a fuller understanding of the prevalence and mechanisms of sensory bias.

Fisherian runaway and sexy sons hypothesis

These hypotheses refer to a coupled selection for females to be attracted and, likewise, a selection for males to be attractive. This can lead to self-reinforcing coevolution. If runaway selection is strong enough, it may incur significant costs such as increased visibility to predators and energetic costs to maintain the trait's full expression. Hence peacocks' extravagant feathers, or any number of lek mating displays. This model does not predict a genetic benefit; rather, the reward is more mates.

In a study done on great reed warblers, models based on the polygyny threshold and sexy son hypotheses predict that females should gain evolutionary advantage in either short-term or long-term in this mating system. Although the importance of female choice was demonstrated, the study did not support the hypotheses. Other studies, such as those conducted on long-tailed widowbirds, have demonstrated the existence of female choice. Here, females chose males with long tails, and even preferred those males with experimentally lengthened tails over shortened tails and those of naturally occurring length. Such a process shows how female choice could give rise to exaggerated sexual traits through Fisherian runaway selection.

Indicator traits

Indicator traits are those that signal good overall quality of the individual. Traits that are perceived as attractive must reliably indicate broad genetic quality in order for selection to favor them and for preference to evolve. This is an example of indirect genetic benefits received by the choosy sex because mating with such individuals will result in high quality offspring. The indicator traits hypothesis is split into three highly related subtopics: the handicap theory of sexual selection, the good genes hypothesis, and the Hamilton-Zuk hypothesis.

People rate the importance of certain traits differently when referring to their own or to others ideal long term partner's. Research suggests that women consider traits indicating genetic fitness as more important for their own partner, and traits that provide benefits to others are proritised for their sister's ideal partner.

Indicator traits are condition-dependent and have associated costs. Therefore, individuals that can handle these costs well (cf. "I can do X [here, survive] with one hand tied behind my back") should be desired by the choosy sex for their superior genetic quality. This is known as the handicap theory of sexual selection.

The good genes hypothesis states that the choosy sex will mate with individuals who possess traits that signify overall genetic quality. In doing so, they gain an evolutionary advantage for their offspring through indirect benefit.

The Hamilton-Zuk hypothesis posits that sexual ornaments are indicators of parasite and disease resistance. To test this hypothesis, red jungle fowl males were infected with a parasitic roundworm and monitored for growth and developmental changes. Female preference was also evaluated. What the researchers found was that parasites affected the development and final appearance of ornamental traits and that females preferred males who were not infected. This supports the idea that parasites are an important factor in sexual selection and mate choice.

One of many examples of indicator traits is the condition-dependent patch of red feathers around the face and shoulders of the male house finch. This patch varies in brightness among individuals because the pigments that produce the red color (carotenoids) are limited in the environment. Thus, males who have a high quality diet will have brighter red plumage. In a manipulation experiment, female house finches were shown to prefer males with brighter red patches. Also, males with naturally brighter patches were better fathers and exhibited higher offspring feeding rates than duller males. This study is heavily cited in the literature and it provides solid support for the indicator traits hypothesis that is associated with direct benefits.

Genetic compatibility

Genetic compatibility refers to how well the genes of two parents function together in their offspring. Choosing genetically compatible mates could result in optimally fit offspring and notably affect reproductive fitness. However, the genetic compatibility model is limited to specific traits due to complex genetic interactions (e.g. major histocompatibility complex in humans and mice). The choosy sex must know their own genotype as well as the genotypes of potential mates in order to select the appropriate partner. This makes testing components of genetic compatibility difficult and controversial.

A controversial but well known experiment suggests that human females use body odor as an indicator of genetic compatibility. In this study, males were given a plain T-shirt to sleep in for two nights in order to provide a scent sample. College women were then asked to rate odors from several men, some with similar MHC (major histocompatibility complex) genes to their own and others with dissimilar genes. MHC genes code for receptors that identify foreign pathogens in the body so that the immune system may respond and destroy them. Since each different gene in the MHC codes for a different type of receptor it is expected that females will benefit from mating with males who have more dissimilar MHC genes. This will ensure better resistance to parasites and disease in the offspring. Researchers found that women tended to rate the odors higher if the male's genes were more dissimilar to their own. They conclude that the odors are influenced by the MHC and that they have consequences for mate choice in human populations today.

Similar to the humans of the odor rating experiment, animals also choose mates based upon genetic compatibility as determined by evaluating their potential mate(s) body odor. Some animals, such as mice even assess a mate's genetic compatibility based on their urine odor.

In an experiment studying three-spined sticklebacks, researchers found that females prefer to mate with males that share a greater diversity of major histocompatibility complex (MHC) and in addition possess a MHC halotype specific to fighting the common parasite Gyrodactylus salaris. Mates that have MHC genes different from one another will be superior when reproducing with regard to parasite resistance, body condition and reproductive success and survival.

The genetic diversity of animals and life reproductive success (LRS) at the MHC level is optimal at intermediate levels rather than at its maximum, despite MHC being one of the most polymorphic genes. In a study, researchers discovered that mice heterozygous at all MHC loci were less resistant than mice homozygous at all loci to salmonella, so it appears disadvantageous to display many different MHC alleles due to the increased loss of T-cells, which aid an organism's immune system and trigger its appropriate response.

MHC diversity may also be correlated to MHC gene expression. As long as a heritable component exists in expression patterns, natural selection is able to act upon the trait. Therefore, gene expression for MHC genes might contribute to the natural selection processes of certain species and be in fact evolutionarily relevant. For example, in another study of three-spined sticklebacks, exposure to parasite species increased MHC class IIB expression by over 25%, proving that parasitic infection increases gene expression.

MHC diversity in vertebrates may also be generated by the recombination of alleles on the MHC gene.

Sex role reversal in animals

In species where mating biases exist, females are typically the choosy sex because they provide a greater parental investment than males. However, there are some examples of sex role reversals where females must compete with each other for mating opportunities with males. Species that exhibit parental care after the birth of their offspring have the potential to overcome the sex differences in parental investment (the amount of energy that each parent contributes per offspring) and lead to a reversal in sex roles. The following are examples of male mate choice (sex role reversal) across several taxa.

Speciation

For many years it has been suggested that sexual isolation caused by differences in mating behaviours is a precursor for reproductive isolation (lack of gene flow), and consequently speciation, in nature. Mate choice behaviours are thought to be important forces that can result in speciation events because the strength of selection for attractive traits is often very strong. Speciation by this method occurs when a preference for some sexual trait shifts and produces a pre-zygotic barrier (preventing fertilisation). These processes have been difficult to test until recently with advances in genetic modelling. Speciation by sexual selection is gaining popularity in the literature with increasing theoretical and empirical studies.

There is evidence of early speciation through mate preference in guppies. Guppies are located across several isolated streams in Trinidad and male colour patterns differ geographically. Female guppies have no coloration but their preference for these colour patterns also vary across locations. In a mate choice study, female guppies were shown to prefer males with colour patterns that are typical of their home stream. This preference could result in reproductive isolation if two populations came into contact again.

The black-throated blue warbler, a North American bird, is another example. Asymmetric recognition of local and non-local songs has been found between two populations of black-throated blue warblers in the United States, one in the northern United States (New Hampshire) and the other in the southern United States (North Carolina). Males in the northern population respond strongly to the local male songs but relatively weakly to the non-local songs of southern males. In contrast, southern males respond equally to both local and non-local songs. The fact that northern males exhibit differential recognition indicates that northern females tend not to mate with "heterospecific" males from the south; thus it is not necessary for the northern males to respond strongly to the song from a southern challenger. A barrier to gene flow exists from South to North as a result of the female choice, which can eventually lead to speciation.

Mate choice in humans

In humans, males and females differ in their strategies to acquire mates and focus on certain qualities. The strategies that each gender uses differs in regards to whether they are long-term or short-term. Human mate choice depends on a variety of factors, such as genes, negative traits, and parasite stress.

Female mate choice

Although, in humans, both males and females are choosy in terms of whom they decide to mate with, as is seen in nature, females exhibit even more mate choice selection than males. According to Bateman's principle of Lifespan Reproductive Success (LRS), human females display the least variance of the two sexes in their LRS due to their high obligatory parental investment, that is a nine-month gestational period, as well as lactation following birth in order to feed offspring so that their brain can grow to the required size.

Historically, human female sexual selection can be examined by looking at ways in which males and females are sexually dimorphic, especially in traits that serve little other evolutionary purpose. For example, male traits such as the presence of beards, overall lower voice pitch, and average greater height are thought to be sexually selected traits as they confer benefits to either the women selecting for them, or to their offspring. Experimentally, women have reported a preference for men with beards and lower voices.

Female mate choice hinges on many different coinciding male traits, and the trade off between many of these traits must be assessed. The ultimate traits most salient to female human mate choice, however, are parental investment, resource provision and the provision of good genes to offspring. Many phenotypic traits are thought to be selected for as they act as an indication of one of these three major traits. The relative importance of these traits when considering mate selection differ depending on the type of mating arrangement females engage in. Human women typically employ long term mating strategies when choosing a mate, however they also engage in short term mating arrangements, so their mate choice preferences change depending on the function of the type of arrangement.

Short term mating strategies

Women do not always seek out and engage in long term mating arrangements. This is evidenced by factors such as the evolved male tendency to seek out multiple sexual partners - a trait that could not have evolved if women were not also historically engaging in short term arrangements - and by the tendency of some women to pursue affairs outside of their long-term couple pairings.

David Buss outlines several hypotheses as to the function of women's short term mate choices:

Long term mating strategies

In long term mating arrangements, women typically look for males who will provide a high level of parental investment, and who can provide resources to the woman or to her offspring. The provision of economic resources, or the potential to acquire many economic resources is the most obvious cue towards the ability of a man to provide resources, and women have been shown experimentally to rate the importance of their partner's financial status twice as highly as men. However, many other traits exist that may act as cues towards a man's ability to provide resources that have been sexually selected for in women's evolutionary history. These include older age – older males have had more time to accrue resources - industriousness, dependability and stability – if a woman's long term partner is not emotionally stable or is not dependable then their provision of resources to her and her offspring are likely to be inconsistent. Additionally, the costs associated with an emotionally unstable partner such as jealousy and manipulativeness may outweigh the benefits associated with the resources they are able to provide.

Women's mate choice is not as straightforward as selecting a mate that displays all of her desired qualities. Often, potential mates will possess some qualities that are desirable and some that are not, so women must assess the relative costs and benefits of their potential partners' traits and 'trade off'. Women's mate choices will also be constrained by the context in which they are making them, resulting in conditional mate choices. Some of the conditions that may influence female mate choice include the woman's own perceived attractiveness, the woman's personal resources, mate copying and parasite stress.

Male mate choice

Generally, it is unusual for males within a species to be the choosy sex. There are many reasons for this. In humans, following sexual reproduction, the female is obliged to endure a nine-month pregnancy and childbirth. This means that females naturally provide a greater parental investment to offspring, than males. Human males have a larger quantity of gametes than females, which are replenished at a rate of approximately 12 million per hour. Conversely, female humans are born with a fixed amount of egg cells which are not restocked over the lifespan. This provides males with a greater window of opportunity to mate and reproduce than females, hence why females are usually more choosy.

Despite not being the typically choosy gender, human males can be influenced by certain traits of females when making decisions about a potential mate:

Short term mating strategies

When finding a short term mate, males highly value women with sexual experience and physical attractiveness. Men seeking short term sexual relationships are likely to avoid women who are interested in commitment or require investment.

Examples of short term mating strategies in males:

Long term mating strategies

Although from an evolutionary perspective women are usually the choosy sex, if a human male has the desire to reproduce he may seek certain qualities in a potential mate who could be the mother of his offspring. Humans have the ability to rely on biological signals of reproductive success and non-biological signals, such as the female's willingness to marry. Unlike many animals, humans are not able to consciously display physical changes to their body when they are ready to mate, so they have to rely on other forms of communication before engaging in a consensual relationship.

Examples of long term mating strategies in males:

Parasite-stress on human mate choice

The parasite-stress theory, otherwise known as pathogen stress, is where a parasite or disease stresses the development of organisms, leading to a change in their mate preference and choice. In societies with a high prevalence of parasites or pathogens greater emphasis is placed by the members of that society, on the physical attractiveness/good looks of their mates or potential mates, compared to members of societies with a lower prevalence of parasites or diseases who put less emphasis on physical attractiveness. It indicates that physical attractiveness is a way in which humans can determine resistance to parasites, as it's believed that parasites and diseases would worsen the look of those who are suffering or have suffered from a disease, and would also limit the number of high-quality pathogen-resistant mates.

Hamilton-Zuk hypothesis

The Hamilton-Zuk hypothesis (see Indicator traits) has greatly influenced research into human mate choice. It has been found that males of all cultures have been found to rate female attractiveness very highly, but when the risk of parasitic infection was high, males rated female attractiveness as much higher. Cultures where parasitic infection is especially high, members of that society use every cue available to them to determine the physical health status of the potential mate. Regardless of the wealth or ideology, the areas of a society i.e. that are more at risk or have higher rates of parasites and diseases, the females will rate masculinity as higher.

Criticisms

Gangested and Buss (2009) say that whilst research indicates that parasite stress may have only influenced mate choice, females searching for "good genes" which show parasite resistance,in areas which have high prevalence of parasites. John Cartwright also points out that females may be simply avoiding the transmission of parasites to themselves rather than it being them choosing males with good genes and that females look for more than just parasite-resistant genes.

MHC-correlated

Major Histocompatibility Complex (MHC) or in humans, Human Leukocyte Antigen (HLA), produce protein products that are essential for the functioning of the immune system. The genes of MHC have extremely high variability, assumed to be a result of frequency-dependent parasite-driven selection and mate choice. This is believed to be so it promotes heterozygosity improving the chances of survival for the offspring and avoid inbreeding.

Odour preferences

In experiments using rats, MHC-associated mate choice indicated that odor cues played a role. In humans, it has generally been shown that a correlation men and women will rate the opposite genders odour as more pleasant, if the human has MHC-dissimilar antigens to them. However, women on contraceptive pills rate the odour of MHC-similar men as being more pleasant, it is unknown why women on contraceptive pills rate smell in this way. It was found that when processing MHC-similar smells were processed faster.

Facial preferences

Human facial preferences have been shown to correlate with both MHC-similarity and MHC-heterozygosity. Research into MHC-similarity with regards to facial attractiveness is limited but research so far suggests that women when thinking of long-term relationships will choose males who are MHC-similar. While facial asymmetry hasn't been correlated with MHC-heterozygosity, the perceived healthiness of skin appears to be. It appears to be that only MHC-heterozygosity and no other genetic markers are correlated with facial attractiveness in males and it has been shown that so far that there is no correlation that has been found in females.