Sexual mimicry

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Sexual mimicry occurs when one sex mimics the opposite sex in its behavior, appearance, or chemical signalling.

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It is more commonly seen within invertebrate species, although sexual mimicry is also seen among vertebrates such as spotted hyenas.

Sexual mimicry is commonly used as a mating strategy to gain access to a mate, a defense mechanism to avoid more dominant individuals, or a survival strategy. It can also be a physical characteristic that establishes an individual's place in society. Sexual mimicry is employed differently across species and it is part of their strategy for survival and reproduction.

Examples of intraspecific sexual mimicry in animals include the spotted hyena, certain types of fish, passerine birds and some species of insect.

Interspecific sexual mimicry can also occur in some plant species, especially orchids. In plants employing sexual mimicry, flowers mimic mating signals of their pollinator insects. These insects are attracted and pollinate the flowers through pseudocopulations or other sexual behaviors performed on the flower.

Social systems

Sexual mimicry can play a role in the development of a species' social system. Perhaps the most extreme example of this can be seen in the spotted hyena, Crocuta crocuta. [1] Female hyenas of all ages possess pseudomasculinized genitalia, including a pseudopenis formed from the clitoris, and a false scrotum formed from the labia. These characteristics likely initially evolved to reduce rates of intrasex aggression received by cub and juvenile females from adult females. However, the trait has evolved beyond its initial use to become highly relevant to spotted hyena communication. Subordinate hyenas will greet dominant individuals by erecting their penis or pseudopenis and allowing the dominant individual to lick it. This likely initially evolved as a means of discerning the sex of the subordinate individual, as the pseudopenis less closely resembles a genuine penis when erect, and tasting the area could allow for the detection of sex specific hormone concentrations. However, this behaviour continues to be engaged in by adult, parous females which no longer convincingly resemble males, visually or olifactorily.

Mating systems

In the spotted hyenas, the only way for the males to mate with the females is if they have the female's full cooperation because of the female's peniform clitoris. An increase in the male's status gave them more access to dominant females in the clan. Non-dominant females are observed copulating more often with lower-ranking males. [2] It is costly for female hyenas to give birth through their long peniform clitoris. The umbilical cord is 12–18 cm long, while the journey from the uterus to the clitoris end is 40 cm. The umbilical cord often breaks before the cub emerges, leading to death by anoxia for many young. This journey is not only harmful for the cubs, but also for the mother. The tissue of the clitoris will sometimes rip open when giving birth for the first time which can be fatal to the mother. [3]

Sexual mimicry is also used as a mate-guarding strategy by some species. Mate-guarding is a process in which a member of a species prevents another member of the same species from mating with their partner. Mate-guarding is seen in Cotesia rubecula , a parasitic wasp from the family Braconidae whose mating system is polygynous. Males are attracted to females through pheromones and they induce females to mate through vibrations, to which the female responds by assuming a specific position. When a male who has copulated with a female sees another male trying to court her, he will often adopt the female receptive position. Post-copulatory female mimicry by the male offers an advantage by acting as a mate-guarding mechanism. If a second male arrives soon enough after the female copulates with the first male, the second male may be able to induce a second copulation which will compete with the first one. However, if the first male who copulated with her mimics the female, it distracts the second male long enough that the female becomes unreceptive. [4]

Sneaky copulation

Salaria pavo female Salaria pavo female 2009 G4.jpg
Salaria pavo female
Salaria pavo male Salaria pavo male 2009 G2.jpg
Salaria pavo male

Sneaky copulation is a strategy used by many aquatic organisms who portray sexual mimicry. Several studies have found that small male fish will look and behave like the female of their species in order to gain access to female territory and copulate with them. [5] [6] In the fish family Blenniidae, the female Salaria pavo will show a specific colour pattern and movement when they want to approach a male and copulate with him. The male guards a territory, and when the female lays her eggs, the parental male protects that territory until the eggs hatch. A second type of males, the sneaker males, is parasitic and resembles the female bleniid fish in their small size, colour, and movement patterns. This allows them to intrude into the nest guarded by the parental males. Sneaker males approach the nests with the same colour patterns and movements that the females hold. Most cases of sneaker males are seen when there is a female already inside the nest although sometimes the sneaker fish enters the nest alongside a female. This species of fish releases the sperm before the female releases her eggs into the water [7] making it possible for the sneaker fish to fertilize an egg, even if the female is not present in the nest. [5]

Sepia apama Sepia apama.jpg
Sepia apama

In the Sepiina family, the giant cuttlefish, Sepia apama, have some males that are large and able to guard a female's nest while other males are small and resemble females in order to sneak in copulations. In the giant cuttlefish, the male courts the female and transfers its sperm to a pouch below the female's beak. During this process, the female displays a body pattern of black splotches on a white background. Once the eggs are laid, the male guards the nest from any possible suitors and opponents. A ‘second female’ is sometimes seen during male-female interaction in close proximity to the couple. This female-looking cuttlefish has the same black blotches as a real female. If the male leaves to fight other males, this individual approaches the female and copulates with her, usually with success. However, in the absence of rivals, these 'mimicking female' males display the phenotype of a mature male. [6]

Sexual mimicry against aggression

A similar phenomenon to the sneaker fish males is observed in the dark-edged splitfin, Girardinichthys multiradiatus. The juveniles resemble the pregnant females in the species by having a dark spot near the vent. In this case, however, the mimicking males have the capability to resemble the females or become a morphologically mature male throughout most of their adult life. This dark spot allows the female-looking males to escape aggression from more dominant males, as well as reducing the chance of having a female nearby flee due to persisting courting males. The mature males do not attack the subordinate fish and the subordinate fish decides when to initiate the fights, which gives it an advantage as the mature male is not expecting this. The dark spot also permits access of subordinate males to females, a characteristic that is advantageous because females' eggs can only be fertilized during a five-day fertilizing window. [8]

Male Ficedula hypoleuca Ficedula hypoleuca Sussex 2.jpg
Male Ficedula hypoleuca
Female/juvenile Ficedula hypoleuca Ficedula hypoleuca Sussex 8.jpg
Female/juvenile Ficedula hypoleuca

Sexual mimicry to avoid aggression is also seen in birds. In some bird species, males have a female-like plumage colour during their second year of life (SY males). These SY males are sexually mature and able to breed, but their morphology differs greatly from the older, after second year (ASY) males. Various studies have looked into this delayed plumage maturation (DPM) and found that the DPM in SY males reduces aggression from ASY males. [9] [10] [11] Female mimicry in birds was first found in European pied flycatcher, Ficedula hypoleuca. When a dull-coloured male is in the area, mature males reduce their aggressiveness and behave as if the intruder is a female. The dull plumage is seen mostly in younger males, likely due to being born later in the previous spring. The resemblance to females benefit these young males when trying to occupy a territory with many males already present because the young males can gain information and access to a territory that would not be accessible to them otherwise. [10]

There is a big cost to not looking like a male when it comes to defending a territory or attracting a mate. Females show aggression against dull-coloured males, making it harder for them to mate. [10] However, DPM has some benefits: as mentioned above, it reduces aggression from older males. [10] As well, these female-looking birds are able to get access to territories, mates, and food that may be not be available to them otherwise. Another benefit is that DPM provides SY birds with a longer lifespan; because they do not have to compete with other males, their mortality rate is lower. This advantage, however, only benefits individuals of species that have a longer potential lifespan and, therefore, DPM would not benefit a short-lived species. [9] This is known as the breeding threshold hypothesis, and states that SY males should only delay breeding if there is a large mortality difference between the SY males who attempt to breed and the ones who do not. [9]

Platysaurus broadleyi Platysaurus broadleyi01.jpg
Platysaurus broadleyi

Most studies addressed DPM as a type of sexual mimicry, [9] [10] which is done through deception: male ASY birds should not be able to tell females or SY males apart. However, Muheter et al. (1997) found that territorial males perceive the dull-coloured males as males but they show less aggression because their dull-coloured plumage promotes low competitive ability. They referred to this as honest signalling and not sexual mimicry. [11]

Another example of sexual mimicry occurs in Broadley's Flat Lizard, Platysaurus broadleyi, where some males mimic females. Flat lizard males tend to be territorial and aggressive towards other males. Therefore, it is beneficial for some males to mimic females in order to avoid aggressive encounters and move freely through the male's territory, looking for mates. There are two types of males in this population; she-males, who mimic females, and he-males, who look like males. The she-males can visually fool the he-males into believing that they are female due to their female morphology. However, the she-males cannot fool the he-males through scent, as he-males can detect the difference. Therefore, the most successful she-males are those who avoid close contact with other males, thereby reducing the chances of detection through chemical signals. [12]

Molecular control over sexual mimicry

In a lekking shorebird species, the ruff, or Philomachus pugnax, there are three distinct male morphs: independent males, the primary, dark-feathered morph, which establishes and aggressively defends a lekking territory, satellite males, a light-feathered morph which does not defend its own territory but which seeks prominent independent males to display alongside, and faeder males, which lack the typical male breeding plumage, instead more closely resembling females, possess a smaller body size, intermediate between a typical male and female, and which do not consistently occupy a single territory, but move freely between different independent male territories, perhaps owing to their female-like plumage, and engage in sneak copulations with females. [13]

When testosterone is administered to reeves (female ruffs), male courtship behaviour and male feather colouration are expressed in the reeves. Testosterone, in this case, expresses sex-limited characteristics by acting on the single autosomal gene. [14]

Biology Illustration Animals Insects Drosophila melanogaster Biology Illustration Animals Insects Drosophila melanogaster.svg
Biology Illustration Animals Insects Drosophila melanogaster

A different example is seen in mature female fruit flies, Drosophila melanogaster , who are very attractive but their level of attractiveness decreases by half or more after three minutes of mating. [15] Males release a compound, 7-tricosene, into the female during courtship that lowers female attractiveness. However, the researcher found that the females release this compound as well, six hours after mating. This compound lowers the female's levels of attractiveness both times, when the male is courting her and during mating. This way, the female mimics the male and with this compound, she lowers her levels of attractiveness. [16]

Genetic control over sexual mimicry

Paracerceis sculpta (Marine isopod) Paracerceis sculpta illustration.png
Paracerceis sculpta (Marine isopod)

Some organisms' sexual mimicry is genetically determined by specific alleles. In the marine isopod, Paracerceis sculpta , there are three different male morphologies: the alpha male is the largest morph, it matures last, and it is the one who gets privileged access to the females. The beta male is of intermediate size, and it mimics the female to get access to females. Last, the gamma male is the smallest morph and it invades harems, where females go to mate with alpha males, for mating opportunities. This morphology is associated with a single autosomal gene and three different alleles. Beta is the most dominant allele, followed by gamma, which is followed by alpha. Selection on these alleles acts according to the Hardy-Weinberg equilibrium and mating success is equivalent among all three morphs. [17]

The alpha males, who are homozygous for the alpha allele, mate with many females in a harem. The females prefer to aggregate with other females in the harem, which gives the alpha male a bigger selection of mating partners. Shuster (1992) looked at the behaviour and relationship of each morph with respect to the harem and found that beta and gamma males could locate harems that have sexually receptive females. They were also able to differentiate between a harem with a sexually receptive female, i.e. one that is able to mate, and a non-sexually receptive female, i.e. one that has already deposited the embryo into her pouch and can no longer mate. While it is still unclear how the beta males do this or how their mating strategies work, they are not harassed by alpha males due to their mimicry of females: the beta males can attract other females into the harem since females like to go where other females are, and this provides the alpha males with more mates. [18]

Another order of organisms whose sexual mimicry is influenced by their DNA is the Odonata, carnivorous insects known as dragonflies and damselflies. In these species, it is the female who sometimes mimics the male. Within a species, groups of females will differ in colour: one group mimics the males' colour and they are known as androchromes. Other groups will have their own female colouration and they are known as gynochromes. In Ischnura elegans , androchromes comprise 6-30% of the female population and their colour is usually blue, like the males; in some populations, androchromes are larger in size than gynochromes. This polymorphism is controlled by an autosomal allele and some studies have looked at the reason for the polymorphism's maintenance. [19]

Aeshna affinis Male Aeshna affinis qtl4.jpg
Aeshna affinis Male
Aeshna affinis Female Androchrome AeshnaAffinisFemaleAndrochrome.jpg
Aeshna affinis Female Androchrome

The most likely theory for the maintenance of the polymorphism in Odonata is the density dependence theory [20] that states that at a high male density, the androchromes are not bothered by the males and their existence is not threatened by male harassment. This hypothesis also assumes that males cannot distinguish between androchromes and other males. This advantage, however, is counteracted with the fact that they will not get a lot of mating opportunities (if any) and their reproduction is limited. This theory is the most likely explanation for the maintenance of polymorphism, since studies have shown that there is an advantage for androchromes in high male-density populations. [21]

In the swordtail fish Xiphophorus birchmanni , 40% of males develop a "false gravid spot," a trait that allows males to mimic the "pregnancy spot" found in females. [22] The false gravid spot is caused by structural variation which up-regulates expression of the nearby gene kit-ligand. [22] Males with the spot experience reduced aggression from other males; however, they are disdained by females but receive more attention from males. [22]

Self-control over sexual mimicry

While, as seen before, most organisms which portray sexual mimicry are born with this morphology/behaviour, this is not always the case. The giant cuttlefish, Sepia apama, mentioned above in the section “sneaky copulations”, is born with the capacity to choose whether to change its morphology to look like a female or a mature male. When no competition is seen nearby, the cuttlefish will look like a mature male and mate with the female. However, when a mature male and a female are copulating, the giant cuttlefish will resemble a female and stay at a close distance of the couple, hoping for a chance to mate with the female if the mature male leaves to fight other males. [6] Another example of an organism that has the capability to remain small and look like a female, or become a morphologically mature male, is the dark-edged splitfin, Girardinichthys multiradiatus. The purpose for their female mimicry was seen before, in the “sexual mimicry against aggression” section where the female-looking males will escape aggression from dominant males and avoid females fleeing their company due to persisting courting males. [8]

Interspecific deceptive mimicry

Bee Orchid Bee Orchid - geograph.org.uk - 852335.jpg
Bee Orchid

Interspecific sexual mimicry can also occur in some plant species. The most common example of this is known as sexually deceptive pollination and is found among some orchids. [23] The orchid mimics its pollinator's females, usually hymenopterans such as wasps and bees, attracting the males to the flower. Orchid flowers mimic the sex pheromones and to some degree the visual appearance of the female insect of its pollinator species. The primacy of olfactory over visual cues has been demonstrated in many cases, such as in the European orchid genus Ophrys as well as many Australian sexually deceptive orchids. In few other cases, such as the South African daisy Gorteria diffusa , visual signals seem to be of primary importance. [24] Visual signals also enhance the attractiveness of the flowers of some Ophrys species to their pollinators. [25] [26] Some male scoliid wasps such as Campsoscolia ciliata are more attracted to the Ophrys flowers' odours than to the odours of the female wasps, although they both attract the males with the same compounds. This is most likely a result of a higher amount of scent coming from the orchid flowers; female wasps tend to produce less scent to avoid attracting predators. [27] Regardless of whether orchids use appearances, fragrances or both, they mimic the female pollinator for their own benefit.

See also

Related Research Articles

<span class="mw-page-title-main">Sexual selection</span> Mode of natural selection involving the choosing of and competition for mates

Sexual selection is a mode of natural selection in which members of one biological sex choose mates of the other sex to mate with, and compete with members of the same sex for access to members of the opposite sex. These two forms of selection mean that some individuals have greater reproductive success than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring. Successful males benefit from frequent mating and monopolizing access to one or more fertile females. Females can maximise the return on the energy they invest in reproduction by selecting and mating with the best males.

<span class="mw-page-title-main">Sexual dimorphism</span> Condition where males and females exhibit different characteristics

Sexual dimorphism is the condition where sexes of the same species exhibit different morphological characteristics, particularly characteristics not directly involved in reproduction. The condition occurs in most dioecious species, which consist of most animals and some plants. Differences may include secondary sex characteristics, size, weight, color, markings, or behavioral or cognitive traits. Male-male reproductive competition has evolved a diverse array of sexually dimorphic traits. Aggressive utility traits such as "battle" teeth and blunt heads reinforced as battering rams are used as weapons in aggressive interactions between rivals. Passive displays such as ornamental feathering or song-calling have also evolved mainly through sexual selection. These differences may be subtle or exaggerated and may be subjected to sexual selection and natural selection. The opposite of dimorphism is monomorphism, when both biological sexes are phenotypically indistinguishable from each other.

<span class="mw-page-title-main">Mimicry</span> Imitation of another species for selective advantage

In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. Often, mimicry functions to protect a species from predators, making it an anti-predator adaptation. Mimicry evolves if a receiver perceives the similarity between a mimic and a model and as a result changes its behaviour in a way that provides a selective advantage to the mimic. The resemblances that evolve in mimicry can be visual, acoustic, chemical, tactile, or electric, or combinations of these sensory modalities. Mimicry may be to the advantage of both organisms that share a resemblance, in which case it is a form of mutualism; or mimicry can be to the detriment of one, making it parasitic or competitive. The evolutionary convergence between groups is driven by the selective action of a signal-receiver or dupe. Birds, for example, use sight to identify palatable insects and butterflies, whilst avoiding the noxious ones. Over time, palatable insects may evolve to resemble noxious ones, making them mimics and the noxious ones models. In the case of mutualism, sometimes both groups are referred to as "co-mimics". It is often thought that models must be more abundant than mimics, but this is not so. Mimicry may involve numerous species; many harmless species such as hoverflies are Batesian mimics of strongly defended species such as wasps, while many such well-defended species form Müllerian mimicry rings, all resembling each other. Mimicry between prey species and their predators often involves three or more species.

<span class="mw-page-title-main">Pseudocopulation</span> Biological process

Pseudocopulation describes behaviors similar to copulation that serve a reproductive function for one or both participants but do not involve actual sexual union between the individuals. It is most generally applied to a pollinator attempting to copulate with a flower. Some flowers mimic a potential female mate visually, but the key stimuli are often chemical and tactile. This form of mimicry in plants is called Pouyannian mimicry.

<span class="mw-page-title-main">Polymorphism (biology)</span> Occurrence of two or more clearly different morphs or forms in the population of a species

In biology, polymorphism is the occurrence of two or more clearly different morphs or forms, also referred to as alternative phenotypes, in the population of a species. To be classified as such, morphs must occupy the same habitat at the same time and belong to a panmictic population.

Frequency-dependent selection is an evolutionary process by which the fitness of a phenotype or genotype depends on the phenotype or genotype composition of a given population.

<span class="mw-page-title-main">Blue-tailed damselfly</span> Species of damselfly

The blue-tailed damselfly or common bluetail is a damselfly, belonging to the family Coenagrionidae.

<span class="mw-page-title-main">Common side-blotched lizard</span> Species of lizard

The common side-blotched lizard is a species of side-blotched lizard in the family Phrynosomatidae. The species is native to dry regions of the western United States and northern Mexico. It is notable for having a unique form of polymorphism wherein each of the three different male morphs utilizes a different strategy in acquiring mates. The three morphs compete against each other following a pattern of rock paper scissors, where one morph has advantages over another but is outcompeted by the third.

<span class="mw-page-title-main">Long-tailed paradise whydah</span> Species of bird

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<i>Hymenopus coronatus</i> Species of praying mantis

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A pseudo-penis is any structure found on an animal that, while superficially appearing to be a penis, is derived from a different developmental path.

<span class="mw-page-title-main">Aggressive mimicry</span> Deceptive mimicry of a harmless species by a predator

Aggressive mimicry is a form of mimicry in which predators, parasites, or parasitoids share similar signals, using a harmless model, allowing them to avoid being correctly identified by their prey or host. Zoologists have repeatedly compared this strategy to a wolf in sheep's clothing. In its broadest sense, aggressive mimicry could include various types of exploitation, as when an orchid exploits a male insect by mimicking a sexually receptive female, but will here be restricted to forms of exploitation involving feeding. For example, indigenous Australians who dress up as and imitate kangaroos when hunting would not be considered aggressive mimics, nor would a human angler, though they are undoubtedly practising self-decoration camouflage. Treated separately is molecular mimicry, which shares some similarity; for instance a virus may mimic the molecular properties of its host, allowing it access to its cells. An alternative term, Peckhamian mimicry, has been suggested, but it is seldom used.

<i>Papilio dardanus</i> Species of butterfly

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<span class="mw-page-title-main">Mimicry in plants</span>

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References

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  24. ↑ Ellis AG, Johnson SD (November 2010). "Floral Mimicry Enhances Pollen Export: The Evolution of Pollination by Sexual Deceit Outside of the Orchidaceae". The American Naturalist . 176 (5): E143–E151. doi:10.1086/656487. PMID   20843263. S2CID   45076899.
  25. ↑ Gaskett AC, Herberstein ME (2 October 2009). "Colour mimicry and sexual deception by Tongue orchids (Cryptostylis)". Naturwissenschaften . 97 (1): 97–102. doi:10.1007/s00114-009-0611-0. PMID   19798479. S2CID   1729573.
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