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Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon.

ABSTRACT: The female-limited Batesian mimicry polymorphism in Papilio butterflies is an intriguing system for investigating the mechanism of maintenance of genetic polymorphisms. In Papilio polytes, an autosomal region encompassing the sex-determinant gene doublesex controls female-limited mimicry polymorphism. In the closely related species P. memnon, which also exhibits female-limited Batesian mimicry polymorphism, we identified two allelic sequences of the doublesex gene that corresponded exactly with the mimetic and non-mimetic female phenotypes. Thus, the genetic basis of the mimicry polymorphism in P. memnon is similar to that in P. polytes. However, the mimetic and non-mimetic alleles of the two species were not identical, and the divergence of alleles occurred independently in P. memnon and P. polytes. Different mutation-selection processes may have resulted in the convergent patterns of mimicry polymorphism in these Papilio butterflies.

SUBMITTER: Komata S

PROVIDER: S-EPMC5052519 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon.

Komata Shinya S Lin Chung-Ping CP Iijima Takuro T Fujiwara Haruhiko H Sota Teiji T

Scientific reports 20161006

The female-limited Batesian mimicry polymorphism in Papilio butterflies is an intriguing system for investigating the mechanism of maintenance of genetic polymorphisms. In Papilio polytes, an autosomal region encompassing the sex-determinant gene doublesex controls female-limited mimicry polymorphism. In the closely related species P. memnon, which also exhibits female-limited Batesian mimicry polymorphism, we identified two allelic sequences of the doublesex gene that corresponded exactly with ...[more]

PMID: 27708422

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Project description:Papilio butterflies are known to possess female-limited Batesian mimicry polymorphisms. In Papilio memnon, females have mimetic and non-mimetic forms, whereas males are monomorphic and non-mimetic. Mimetic females are characterized by color patterns and tails in the hindwing and yellow abdomens. Recently, an analysis of whole-genome sequences has shown that an approximately 160 kb region of chromosome 25 is responsible for mimicry and has high diversity between mimetic (A) and non-mimetic (a) alleles (highly diversified region: HDR). The HDR includes three genes, UXT, doublesex (dsx), and Nach-like, but the functions of these genes are unknown. Here, we investigated the function of dsx, a gene involved in sexual differentiation, which is expected to be functionally important for hindwing and abdominal mimetic traits in P. memnon. Expression analysis by reverse transcription quantitative PCR (RT-qPCR) and RNA sequencing showed that mimetic dsx (dsx-A) was highly expressed in the hindwings in the early pupal stage. In the abdomen, both dsx-A and dsx-a were highly expressed during the early pupal stage. When dsx was knocked down using small interfering RNAs (siRNAs) designed in the common region of dsx-A and dsx-a, a male-like pattern appeared on the hindwings of mimetic and non-mimetic females. Similarly, when dsx was knocked down in the abdomen, the yellow scales characteristic of mimetic females changed to black. Furthermore, when dsx-a was specifically knocked down, the color pattern of the hindwings changed, as in the case of dsx knockdown in non-mimetic females but not mimetic females. These results suggest that dsx-a is involved in color pattern formation on the hindwings of non-mimetic females, whereas dsx-A is involved in hindwing and abdominal mimetic traits. dsx was involved in abdominal and hindwing mimetic traits, but dsx expression patterns in the hindwing and abdomen were different, suggesting that different regulatory mechanisms may exist. Our study is the first to show that the same gene (dsx) regulates both the hindwing and abdominal mimetic traits. This is the first functional analysis of abdominal mimicry in butterflies.

Project description:BackgroundMimicry, in which one prey species (the Mimic) imitates the aposematic signals of another prey (the Model) to deceive their predators, has attracted the general interest of evolutionary biologists. Predator psychology, especially how the predator learns and forgets, has recently been recognized as an important factor in a predator-prey system. This idea is supported by both theoretical and experimental evidence, but is also the source of a good deal of controversy because of its novel prediction that in a Model/Mimic relationship even a moderately unpalatable Mimic increases the risk of the Model (quasi-Batesian mimicry).Methodology/principal findingsWe developed a psychology-based Monte Carlo model simulation of mimicry that incorporates a "Pavlovian" predator that practices an optimal foraging strategy, and examined how various ecological and psychological factors affect the relationships between a Model prey species and its Mimic. The behavior of the predator in our model is consistent with that reported by experimental studies, but our simulation's predictions differed markedly from those of previous models of mimicry because a more abundant Mimic did not increase the predation risk of the Model when alternative prey were abundant. Moreover, a quasi-Batesian relationship emerges only when no or very few alternative prey items were available. Therefore, the availability of alternative prey rather than the precise method of predator learning critically determines the relationship between Model and Mimic. Moreover, the predation risk to the Model and Mimic is determined by the absolute density of the Model rather than by its density relative to that of the Mimic.Conclusions/significanceAlthough these predictions are counterintuitive, they can explain various kinds of data that have been offered in support of competitive theories. Our model results suggest that to understand mimicry in nature it is important to consider the likely presence of alternative prey and the possibility that predation pressure is not constant.

Dataset Information

Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon.

Publications

Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon.

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