KeywordsDominant Male Territorial Male Virgin Queen Negative Frequency Dependent Selection Reproductive Parasite
Female mimics are males of otherwise sexually dimorphic species that resemble females in appearance and behavior.
In sexually dimorphic species, some males will look more like females than males when it comes to size, coloration, pheromone signaling, and behavior. Such female mimics are widespread across the animal kingdom; they have been described in beetles, ants, mollusks, crustaceans, and every vertebrate class, among others (Oliveira et al. 2008). Taking up the female appearance can be permanent or temporary. In the majority of cases it is a form of deceit to gain competitive advantages, for example, female mimicry is used as an alternative mating strategy by smaller males who otherwise would not be able to mate. In their disguise, the sneaker male can approach females and avoid agonistic interactions by the larger males and frequently manages to steal copulations.
Alternative Mating Strategies
In species with strong sexual selection, matings are often monopolized by very few dominant males. To become dominant, a male typically needs to be large and aggressive. Under these circumstances smaller males hardly ever have the chance to mate. Female mimicry is an alternative mating strategy that enables some males to gain reproductive success. Disguised as a female these males are often not detected by their dominant rivals and can hence avoid aggressive confrontations and eviction from the territory and stay in close proximity of receptive females that have been attracted to the dominant male. Whether females choose to mate with the sneaker male or cannot avoid the sneaky copulation when attempting to mate with the dominant male is unclear, although the current evidence points towards a preference for the dominant males and female avoidance of sneakers where possible (Oliveira et al. 2008).
The sneaker male will mimic females in many morphological and physiological traits, coloration, and behavior. Pretending to be a female is not restricted to visual effects. In the tropical ant Cardiocondyla obscurior the sneaker male mimics the queen’s chemical bouquet to avoid fights with aggressive males that otherwise often lead to death (Cremer et al. 2002). This chemical mimicry is effective in competition for matings with virgin queens in the nest, which otherwise would be monopolized by the aggressive males. Sneaking behavior and female mimics also have hormonal adaptations; for instance the mimics often have lower levels of testosterone, which is associated with aggressive behavior, than the ordinary males (Cardwell and Liley 1991; Sinervo et al. 2000; Küpper et al. 2016). Female mimics do not express typical male ornaments, nevertheless he always possesses male gonads. The testes of sneaker males are occasionally larger than those of dominant males and may increase its chances of siring offspring during sperm competition (Küpper et al. 2016).
Female mimics have two principal behavioral tactics. They may either try to avoid the attention of the dominant male or stealthily sneak copulation when the dominant male is engaged otherwise. Alternatively, they may actively distract the dominant male from copulations by posing as a receptive female and drawing attention away from the female to themselves. This deceit is very effective and the mimic is frequently mounted by the male who will then waste time, sperm, and energy on the female impersonator.
As other alternative mating strategies, female mimicry is often under negative frequency dependent selection since the deceit is most effective when mimics are rare within a population. By enabling more males to participate in reproduction it reduces the reproductive skew within a population.
Permanent Versus Temporary Female Impersonation
Female mimicry can be expressed permanently or temporary by males. Permanent mimicry is known to have a genetic basis in birds and crustaceans. In the Ruff Philomachus pugnax, the genes responsible for the female mimicry are located within a chromosomal inversion (Küpper et al. 2016). A genetic basis, however, does not necessarily mean that female mimicry is expressed life-long. In the common Side-blotched Lizard Uta stansburiana, female mimics can develop into monogamous territorial males that have higher fitness when the frequency of the sneaker male is high (Sinervo et al. 2000). Temporary female mimics occur in some fish. In the Stoplight Parrotfish Sparisoma viride, individuals change their sex from female to male throughout their lifetime. Large size is required for males to successfully defend a territory and therefore fish start off as a female and become males only once they have grown to the appropriate size. Some male parrotfish maintain the female phenotype despite having already developed male gonads. These males then live temporarily as sneakers on the territories of dominant males until they have grown enough to become a competitive territorial male (Cardwell and Liley 1991). In Pied Flycatchers Ficedula hypoleuca, second year males often retain the juvenile/female plumage since in this disguise they are tolerated by older males and not recognized as competitors, which provides them with advantages in conflicts over resources (Sætre and Slagsvold 1996). Sneaker males of the Giant Cuttlefish Sepia apama can actively change between male and female appearance and behavior within seconds (Hanlon et al. 2005). An example for extreme flexibility is provided by the Mourning Cuttlefish Sepia plangon, where some males have been observed to take up female coloration and patterning only for the parts of his body that is exposed to a male competitor while simultaneously displaying as a male to a female with the other side of its body (Brown et al. 2012).
Female mimicry also occurs in nonbreeding context. Male garter snakes that recently woke up from hibernation in spring produce female pheromones to attract other males. Within the resulting male aggregation the mimics can avoid predation better and increase their own body temperature and hence become mobile quicker (Shine et al.2001).
Female mimicry is an effective deceit strategy of males that is often found in populations with high sexual selection and strong reproductive skew. It increases the fitness of males that otherwise would not be able to mate but is most effective when rare. Female mimics usually don’t display to females and can be seen as reproductive parasites of territorial males that dominate male-male competition. Through morphological, physiological, and behavioral adaptations mimicry increases phenotypic variation.
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