Mate choice
Encyclopedia
Mate choice, or intersexual selection, is an evolutionary process in which selection of a mate depends on attractiveness of its traits. It is one of two components of sexual selection
(the other is male-male competition or intrasexual selection). Darwin first introduced his ideas on sexual selection in 1871 but advances in genetic and molecular techniques have led to major progress in this field recently.
Five mechanisms that explain the evolution of mate choice are currently recognized. They are direct phenotypic benefits, sensory bias, Fisherian runaway, indicator traits, and genetic compatibility. These mechanisms can co-occur and there are many examples of each.
In systems where mate choice exists, one sex is competitive with same-sex members and the other sex is choosy (selective when it comes to picking individuals to mate with). In most species, females are the choosy sex that discriminate amongst competitive males but there are several examples of reversed roles (see below).
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 they appeared to be detrimental to survival and have negative consequences for reproductive success. He 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 some scholars argue today that sexual selection is a form of natural selection.
The next advancement in the field of sexual selection took place decades later when R.A. Fisher first mentioned his ideas on the evolution of female preference through runaway selection in 1915. 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
).
Using Drosophila as a model, Angus J. 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
emphasized its importance in the 1960s and 1970s.
Soon after Williams' revival of the subject, Robert L. Trivers presented his parental investment
theory. Parental investment was defined by Trivers 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 they will provide after birth or hatching. Reformulating Bateman's ideas, Trivers argued that the sex that 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 favors mating biases.
Direct benefits are those that increase the fitness
of the choosy sex through direct material advantages. These benefits include but are not limited to increased territory quality, increased parental care, and protection from predators. There is much support for maintenance of mate choice by direct benefits and it is the least controversial model to explain discriminate mating.
Indirect benefits increase genetic fitness for the offspring. When it appears that the choosy sex does not receive direct benefits from his or her mate, indirect benefits may be the payoff for being selective. Examples of indirect benefits include better genetic quality and more attractive offspring. R. A. Fisher described this less obvious model in a book called The Genetical Theory of Natural Selection. Fisher explained that, through indirect selection, fitter individuals inherit both the genes and the mating preference for some indicator trait. This linkage of an indicator trait and the preference for such trait results in exaggerated phenotypes and is known as Fisherian runaway selection.
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.
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. Although there are a few examples of possible sensory bias, more testing is required to corroborate this mechanism.
Other examples for the sensory bias mechanism include traits in auklets, wolf spiders, and manakins.
The Fisherian runaway process describes a scenario where a trait arises in a population via natural selection but is quickly favored by sexual selection even if it is no longer advantageous. Preferences for these traits are not based on direct or indirect benefits associated with them. Instead, arbitrary preference is what drives a trait's adaptiveness in the population.
The sexy sons hypothesis is slightly different from Fisherian runaway in that the choosy sex does receive an indirect benefit from having a mating preference. Choosing to mate with an attractive individual will result in attractive offspring who inherit the same preference. Thus, the choosy sex will have future fitness benefits from mating with attractive individuals. In a system where females are choosy, this means that they will mate with attractive males in order to produce "sexy sons". This ensures that her offspring will be attractive to other females in the next generation.
Indicator traits are condition-dependent and have associated costs. Therefore, individuals that can handle these costs well 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.
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. In fact, this is what researcher found in the study. 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.
There is evidence of early speciation through mate preference in guppies. Guppies are located across several isolated streams in Trinidad and male color patterns differ geographically. Female guppies have no coloration but their preference for these color patterns also vary across locations. In a mate choice study, female guppies were shown to prefer males with color patterns that are typical of their home stream. This preference could result in reproductive isolation if two populations came into contact again.
Sexual selection
Sexual selection, a concept introduced by Charles Darwin in his 1859 book On the Origin of Species, is a significant element of his theory of natural selection...
(the other is male-male competition or intrasexual selection). Darwin first introduced his ideas on sexual selection in 1871 but advances in genetic and molecular techniques have led to major progress in this field recently.
Five mechanisms that explain the evolution of mate choice are currently recognized. They are direct phenotypic benefits, sensory bias, Fisherian runaway, indicator traits, and genetic compatibility. These mechanisms can co-occur and there are many examples of each.
In systems where mate choice exists, one sex is competitive with same-sex members and the other sex is choosy (selective when it comes to picking individuals to mate with). In most species, females are the choosy sex that discriminate amongst competitive males but there are several examples of reversed roles (see below).
Origins and history
Charles DarwinCharles Darwin
Charles Robert Darwin FRS was an English naturalist. He established that all species of life have descended over time from common ancestry, and proposed the scientific theory that this branching pattern of evolution resulted from a process that he called natural selection.He published his theory...
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 they appeared to be detrimental to survival and have negative consequences for reproductive success. He 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 some scholars argue today that sexual selection is a form of natural selection.
The next advancement in the field of sexual selection took place decades later when R.A. Fisher first mentioned his ideas on the evolution of female preference through runaway selection in 1915. Fifteen years later, he expanded this theory in a book called The Genetical Theory of Natural Selection
The Genetical Theory of Natural Selection
The Genetical Theory of Natural Selection is a book by R.A. Fisher first published in 1930 by Clarendon. It is one of the most important books of the modern evolutionary synthesis and is commonly cited in biology books.-Editions:...
. 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
Fisherian runaway
Fisherian runaway is a model of sexual selection, first proposed by R.A. Fisher in 1915, and expanded upon in his 1930 book The Genetical Theory of Natural Selection, that suggests an explanation for sexual selection of traits that do not obviously increase fitness of survival, based upon a...
).
Using Drosophila as a model, Angus J. Bateman presented experimental evidence that male reproductive success
Reproductive success
Reproductive success is defined as the passing of genes onto the next generation in a way that they too can pass those genes on. In practice, this is often a tally of the number of offspring produced by an individual. A more correct definition, which incorporates inclusive fitness, is the...
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
Bateman's principle
In biology, Bateman's principle is the theory that females almost always invest more energy into producing offspring than males invest, and therefore in most species females are a limiting resource over which the other sex will compete...
and although this was a major finding that added to the work of Darwin and Fisher, it was overlooked until George C. Williams
George C. Williams
Professor George Christopher Williams was an American evolutionary biologist.Williams was a professor emeritus of biology at the State University of New York at Stony Brook. He was best known for his vigorous critique of group selection. The work of Williams in this area, along with W. D...
emphasized its importance in the 1960s and 1970s.
Soon after Williams' revival of the subject, Robert L. Trivers presented his parental investment
Parental investment
In evolutionary biology, parental investment is any parental expenditure that benefits one offspring at a cost to parents' ability to invest in other components of fitness...
theory. Parental investment was defined by Trivers 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 they will provide after birth or hatching. Reformulating Bateman's ideas, Trivers argued that the sex that 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 favors 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 behavior to evolve. Two types of fitness benefits (direct and indirect) are thought to drive the evolutionary mechanisms of mate choice.Direct benefits are those that increase the fitness
Fitness
Fitness may relate to:* Physical fitness, a general state of good health, usually as a result of exercise and nutrition * Cardiorespiratory fitness...
of the choosy sex through direct material advantages. These benefits include but are not limited to increased territory quality, increased parental care, and protection from predators. There is much support for maintenance of mate choice by direct benefits and it is the least controversial model to explain discriminate mating.
Indirect benefits increase genetic fitness for the offspring. When it appears that the choosy sex does not receive direct benefits from his or her mate, indirect benefits may be the payoff for being selective. Examples of indirect benefits include better genetic quality and more attractive offspring. R. A. Fisher described this less obvious model in a book called The Genetical Theory of Natural Selection. Fisher explained that, through indirect selection, fitter individuals inherit both the genes and the mating preference for some indicator trait. This linkage of an indicator trait and the preference for such trait results in exaggerated phenotypes and is known as Fisherian runaway selection.
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
Northern Cardinal
The Northern Cardinal or Redbird or Common Cardinal is a North American bird in the genus Cardinalis. It can be found in southern Canada, through the eastern United States from Maine to Texas and south through Mexico...
, 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.
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. Although there are a few examples of possible sensory bias, more testing is required to corroborate this mechanism.
Other examples for the sensory bias mechanism include traits in auklets, wolf spiders, and manakins.
Fisherian runaway/Sexy sons hypothesis
Both hypotheses refer to a genetic coupling between the preference for a trait and the trait itself. This can lead to self-reinforcing coevolution which may be limited by natural selection due to the cost of possessing a sexually selected trait. Such costs include increased visibility to predators and energetic costs to maintain them.The Fisherian runaway process describes a scenario where a trait arises in a population via natural selection but is quickly favored by sexual selection even if it is no longer advantageous. Preferences for these traits are not based on direct or indirect benefits associated with them. Instead, arbitrary preference is what drives a trait's adaptiveness in the population.
The sexy sons hypothesis is slightly different from Fisherian runaway in that the choosy sex does receive an indirect benefit from having a mating preference. Choosing to mate with an attractive individual will result in attractive offspring who inherit the same preference. Thus, the choosy sex will have future fitness benefits from mating with attractive individuals. In a system where females are choosy, this means that they will mate with attractive males in order to produce "sexy sons". This ensures that her offspring will be attractive to other females in the next generation.
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.Indicator traits are condition-dependent and have associated costs. Therefore, individuals that can handle these costs well 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 (i.e. Major histocompatibility complexMajor histocompatibility complex
Major histocompatibility complex is a cell surface molecule encoded by a large gene family in all vertebrates. MHC molecules mediate interactions of leukocytes, also called white blood cells , which are immune cells, with other leukocytes or body cells...
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. In fact, this is what researcher found in the study. 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.
Male mate choice/Sex role reversal
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.- FishFishFish are a paraphyletic group of organisms that consist of all gill-bearing aquatic vertebrate animals that lack limbs with digits. Included in this definition are the living hagfish, lampreys, and cartilaginous and bony fish, as well as various extinct related groups...
: Some males of the SyngnathidaeSyngnathidaeSyngnathidae is a family of fish which includes the seahorses, the pipefishes, and the weedy and leafy sea dragons. The name is derived from Greek, meaning "fused jaw" - syn meaning fused or together, and gnathus meaning jaws. This fused jaw trait is something the entire family has in common...
(pipefishPipefishPipefishes or pipe-fishes are a subfamily of small fishes, which, together with the seahorses, form the family Syngnathidae.-Anatomy:...
and seahorses) family of fish display high levels of parental care. This is because females will deposit their eggs in a special brooding pouch that the male possesses. She doesn't participate in parental care after this event. The male then has the burden of raising the offspring on his own which requires energy and time. Thus, males in these species must choose among competitive females for mating opportunities. Surveys across multiple species of pipefish suggest that the sex differences in the level of parental care may not be the only reason for the reversal. Mating systems (e. i. monogamy and polygamy) might also heavily influence the appearance of male mate choice. - AmphibianAmphibianAmphibians , are a class of vertebrate animals including animals such as toads, frogs, caecilians, and salamanders. They are characterized as non-amniote ectothermic tetrapods...
: Male poison-arrow frogsGreen and Black Poison Dart FrogDendrobates auratus, also known as the green and black poison dart frog or the green and black poison arrow frog, and sometimes mint poison frog , is a brightly-colored member of the order Anura native to Central America and north-western parts of South America...
(Dendrobates auratus) take on a very active parenting role. Females are lured by the males to rearing sites where they deposit their eggs. The male fertilizes these eggs and accepts the burden of defending and caring for the young until they are independent. Because the male contributes a higher level of parental investment, females must compete for opportunities to leave their eggs with the limited available males. - BirdBirdBirds are feathered, winged, bipedal, endothermic , egg-laying, vertebrate animals. Around 10,000 living species and 188 families makes them the most speciose class of tetrapod vertebrates. They inhabit ecosystems across the globe, from the Arctic to the Antarctic. Extant birds range in size from...
: Male wattled jacanas provide all parental care after the eggs have been laid by the females. This means that the males must incubate the eggs and defend the nest for an extended period of time. Since males invest much more time and energy into the offspring, females are very competitive for the right to lay their eggs in an established nest. - MammalMammalMammals are members of a class of air-breathing vertebrate animals characterised by the possession of endothermy, hair, three middle ear bones, and mammary glands functional in mothers with young...
: There are no confirmed cases of sex role reversed mammals but female spotted hyenaSpotted HyenaThe spotted hyena also known as laughing hyena, is a carnivorous mammal of the family Hyaenidae, of which it is the largest extant member. Though the species' prehistoric range included Eurasia extending from Atlantic Europe to China, it now only occurs in all of Africa south of the Sahara save...
s have peculiar anatomy and behavior that has warranted much attention. Female spotted hyenas are much more aggressive than males due to their high levels of androgens during development. The increased male hormones during development contribute to an enlarged pseudopenis that is involved in mating and birth. Although the anatomical and behavioral roles differ from accepted norms, spotted hyenas are not sex role reversed because the females do not compete with each other for mates.
Speciation by mate choice
For many years it has been suggested that sexual isolation caused by differences in mating behaviors is a precursor for reproductive isolation (lack of gene flow), and consequently speciation, in nature. Mate choice behaviors 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 prezygotic barrier (preventing fertilization). These processes have been difficult to test until recently with advances in genetic modeling. 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 color patterns differ geographically. Female guppies have no coloration but their preference for these color patterns also vary across locations. In a mate choice study, female guppies were shown to prefer males with color patterns that are typical of their home stream. This preference could result in reproductive isolation if two populations came into contact again.