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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 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 Edit

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 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.[1] This article focuses on the latter. Darwin treated natural selection and sexual selection as two different topics although some scholars[attribution needed] 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.[2] 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.[3] 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.[4][5]

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.[6]

Direct and indirect benefits Edit

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 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[7] and it is the least controversial model to explain discriminate mating.[8]

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.[9] 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 Edit

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.[10]

Direct phenotypic benefits Edit

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.[11] 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.[12]

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.[13] 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.

Sensory bias Edit

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.[14]

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.[15] 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.[16]

Other examples for the sensory bias mechanism include traits in auklets,[17] wolf spiders,[18] and manakins.[19]

Fisherian runaway/Sexy sons hypothesis Edit

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.

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.

Studies in Long-tailed Widowbirds have demonstrated the existence of female choice. Studies demonstrated that females actively chose males with long tails, preferring those males with experimentally lengthened tails over shortened tails and those of naturally occurring length. Furthermore, these studies demonstrated that female choice could give rise to extreme sexual traits through Fisherian runaway selection.

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.[2][9] 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.

Indicator traits Edit

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 (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.[20]

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.[21] 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.[22]

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.[23] 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 Edit

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.[24] 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.[25]

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.[26]

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.[27] 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.[28]

The genetic diversity of animals and life reproductive success (LRS) at the MHC level is optimal at intermediate levels rather than at its maximum,[29][30] despite MHC being one of the most polymorphic genes.[31] 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,[32] which aid an organism’s immune system and trigger its appropriate response.[33]

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.[34]

MHC diversity in vertebrates may also be generated by the recombination of alleles on the MHC gene.[35]

Male mate choice/Sex role reversal Edit

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.[36] The following are examples of male mate choice (sex role reversal) across several taxa.

  • Fish: Male fish typically display high levels of parental care (see pipefish, Scissortail sergeant, and seahorses). 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.[37]
  • Amphibian: Male poison-arrow frogs (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.[38]
  • Bird: Bird species are typically biparental in care, and may also be maternal like the Guianan Cock-of-the-rocks, however the reverse may also hold true. 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.[39]
  • Mammal: There are no confirmed cases of sex role reversed mammals but female spotted hyenas have peculiar anatomy and behavior that has warranted much attention.[40] 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.[41] 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.[42]

Speciation by mate choice Edit

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.[43] 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.[44] 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.[45] This preference could result in reproductive isolation if two populations came into contact again.

The North American bird, black-throated blue warblers, is another example. Asymmetric recognition of local and nonlocal 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).[46] Males in the northern population respond strongly to the local male songs but relatively weakly to the nonlocal songs of southern males. In contrast, southern males respond equally to both local and nonlocal 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.

See also Edit

References Edit

  1. Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. John Murray, London.
  2. 2.0 2.1 (1915). The evolution of sexual preference. Eugenic Review 7 (3): 184–192.
  3. (1948). Intra-sexual selection in Drosophila. Heredity 2 (Pt. 3): 349–368.
  4. Williams, G.C. 1966. Adaptation and Natural Selection. Princeton University Press, Princeton, N.J.
  5. Williams, G. C. 1975. Sex and evolution. Princeton University Press, Princeton, N.J.
  6. Trivers, R.L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man, 1871-1971 (pp. 136–179). Chicago, IL: Aldine
  7. (2001). How important are direct benefits of sexual selection?. Naturwissenschaften 88 (10): 401–415.
  8. (2003). The evolution of mate choice and mating biases. Proceedings of the Royal Society B 270 (1515): 653–664.
  9. 9.0 9.1 Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford, Clarendon Press
  10. Andersson, M. 1994. Sexual Selection, Princeton University Press
  11. (1993). Sexual selection when the female directly benefits. Biological Journal of the Linnean Society 48 (3): 187–211.
  12. Moller, A. P. 1994. Sexual selection and the barn swallow. Oxford University Press, Oxford
  13. (1998). Plumage brightness as an indicator of parental care in northern cardinals. Animal Behavior 55: 119–127.
  14. (2002). How sensory drive can promote speciation. Trends in Ecology and Evolution 17 (12): 571–577.
  15. (2002). A possible non-sexual origin of mate preference: are male guppies mimicking fruit?. Proceedings of the Royal Society B 7 (1490): 475–481.
  16. (2005). Sensory bias as an explanation for the evolution of mate preferences. American Naturalist 166 (4): 437–446.
  17. (1998). Heterospecific mating preferences for a feather ornament in least auklets. Behavioral Ecology 9 (2): 187–192.
  18. (1996). Female choice and pre-existing bias: Visual cues during courtship in two Schizocosawolff spiders. Animal Behavior 52: 167–181.
  19. (1996). Phylogenetic tests of alternative intersexual selection mechanisms: Trait macroevolution in a polygynous clade. The American Naturalist 149 (4): 688–692.
  20. (1975). Mate selection – a selection for the handicap. Journal of Theoretical Biology 53 (1): 205–214.
  21. Hamilton W. D., Zuk M. (1982). Heritable true fitness and bright birds: A role for parasites?. Science 218 (4570): 384–387.
  22. (1990). Parasites and mate choice in red jungle fowl. American Zoology 30 (2): 235–244.
  23. (1991). Plumage coloration is a sexually selected indicator of male quality. Nature 350 (6316): 337–339.
  24. (2005). Genetic compatibility and sexual selection. Trends in Ecology and Evolution 20 (4): 157–158.
  25. (1995). MHC-dependent mate preferences in humans. Proceedings: Biological Sciences 260 (1359): 245–249.
  26. Brennan, Peter A., and Frank Zufall. "Pheromonal Communication in Vertebrates." Nature 444.7117 (2006): 308-15.
  27. Eizaguirre, C., et al. "MHC-Based Mate Choice Combines Good Genes and Maintenance of MHC Polymorphism." Molecular ecology 18.15 (2009): 3316-29.
  28. Reusch, Thorsten B. H., et al. "Female Sticklebacks Count Alleles in a Strategy of Sexual Selection Explaining MHC Polymorphism." Nature 414.6861 (2001): 300-2.
  29. Kalbe M, Eizaguirre C, Dankert I et al. “Lifetime reproductive success is maximized with optimal MHC diversity.” Proceedings of the Royal Society B, Biological Sciences 276 (2009): 925–934.
  30. Nowak MA, Tarczyhornoch K, Austyn J.M. “The optimal number of major histocompatibility complex-molecules in an individual.” Proceedings of the National Academy of Sciences USA 89 (1992): 10896–10899.
  31. Woelfing B, Traulsen A, Milinski M, Boehm T. “Does intra-individual MHC diversity keep a golden mean?” Philosophical Transactions of the Royal Society B: Biological Sciences 364 (2009): 117–128.
  32. Ilmonen P., Penn D.J., Damjanovich K., Morrison L., Ghotbi L., Potts W.K. “Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice.” Genetics 176 (2007): 2501–2508. doi:10.1534/genetics.107.074815.
  33. Schad, J., et al. "MHC Class II DRB Diversity, Selection Pattern and Population Structure in a Neotropical Bat Species, Noctilio Albiventris." Heredity 107.2 (2011): 115-26.
  34. Wegner, M., Kalbe, M., Rauch, G., Kurtz, J., Schaschl, H. and Reusch, T. B. H. “Genetic variation in MHC Class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks.” Molecular Ecology 15 (2006): 1153-1164.
  35. Schaschl, H., et al. "Selection and Recombination Drive the Evolution of MHC Class II DRB Diversity in Ungulates." Heredity 97.6 (2006): 427-37.
  36. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ
  37. (1992). Pipefish and seahorses: Are they all sex role reversed?. Trends in Ecology and Evolution 7 (7): 237–241.
  38. (1978). Courtship and parental behavior in a Panamanian poison-arrow frog (Dendrobates auratus). Herpetologica 34 (2): 148–155.
  39. (2005). Sex dimorphism, intrasexual competition and sexual selection in wattled jacana, a sex role reversed shore bird in Panama. The Auk 121 (2): 391–403.
  40. (2000). Sex-role reversal in vertebratesL behavioral and endocrinological accounts. Behavioral processes 51 (1–3): 135–147.
  41. (1987). Androstenedione may organize or activate sex-reversed traits in female spotted hyenas. PNAS 84 (10): 3444–3447.
  42. (1986). Social organization of the spotted hyena II: Dominance and reproduction. Animal behavior 35 (5): 1510–1527.
  43. Mayr, E. 1942. Systematics and Origin of Species, Belknap Press
  44. (2007). Sexual Selection and Speciation. Annual Review of Ecology, Evolution, and Systematics 38: 79–102.
  45. (1995). Geographic variation in female preferences for male traits in Poecelia reticulata. Evolution 49 (3): 456–468.
  46. Colbeck, G.J., Sillett, T.S.; Webster, M.S. (2010). Asymmetric discrimination of geographical variation in song in a migratory passerine. Animal Behaviour 80: 311–318.

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