Parallel evolution of Batesian mimicry supergene in twoPapiliobutterflies,P. polytesandP. memnon

Iijima, Tadako; Kajitani, Rei; Komata, Shinya; Lin, Chung Ping; Sota, Teiji; Itoh, Takehiko; Fujiwara, Haruhiko

doi:10.1126/sciadv.aao5416

Cited by 56 publications

(121 citation statements)

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“…Each year, new systems with tightly linked clusters of genes are discovered, pointing to the importance of supergenes in the evolution of certain classes of complex traits, including mimetic coloration in butterflies, self-incompatibility in plants, mating strategies in birds, mating types in fungus, and social organization in ants [1,2,[7][8][9][10].…”

Section: Resultsmentioning

confidence: 99%

An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

et al. 2020

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Section: Resultsmentioning

confidence: 99%

An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

et al. 2020

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“…The pleiotropic nature of several genes, such as transcription factors, allows co-option of developmental circuits in novel contexts at relatively short timescales [2]. For instance, horns in beetles [3], wings in insects [4,5] and mimicry in butterflies [6][7][8][9][10][11] have resulted from tissue-and developmental stage-specific co-option of existing genes and pathways. Mutations in regulatory regions, synthesis of different gene products by alternative splicing, and mutations in binding sites that enable interactions with new partners, are a few mechanisms by which transcription factors may acquire functions that lead to novel adaptive phenotypes [12,13].…”

Section: Introductionmentioning

confidence: 99%

Tissue-specific developmental regulation and isoform usage underlie the role of doublesex in sex differentiation and mimicry in Papilio swallowtails

2020

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Adaptive phenotypes often arise by rewiring existing developmental networks. Co-option of transcription factors in novel contexts has facilitated the evolution of ecologically important adaptations. doublesex ( dsx ) governs fundamental sex differentiation during embryonic stages and has been co-opted to regulate diverse secondary sexual dimorphisms during pupal development of holometabolous insects. In Papilio polytes , dsx regulates female-limited mimetic polymorphism, resulting in mimetic and non-mimetic forms. To understand how a critical gene such as dsx regulates novel wing patterns while maintaining its basic function in sex differentiation, we traced its expression through metamorphosis in P. polytes using developmental transcriptome data. We found three key dsx expression peaks: (i) eggs in pre- and post-ovisposition stages; (ii) developing wing discs and body in final larval instar; and (iii) 3-day pupae. We identified potential dsx targets using co-expression and differential expression analysis, and found distinct, non-overlapping sets of genes—containing putative dsx- binding sites—in developing wings versus abdominal tissue and in mimetic versus non-mimetic individuals. This suggests that dsx regulates distinct downstream targets in different tissues and wing colour morphs and has perhaps acquired new, previously unknown targets, for regulating mimetic polymorphism. Additionally, we observed that the three female isoforms of dsx were differentially expressed across stages (from eggs to adults) and tissues and differed in their protein structure. This may promote differential protein–protein interactions for each isoform and facilitate sub-functionalization of dsx activity across its isoforms. Our findings suggest that dsx employs tissue-specific downstream effectors and partitions its functions across multiple isoforms to regulate primary and secondary sexual dimorphism through insect development.

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“…To clarify how green and brown pupal coloration occurs via the expression of pigmentation-specific genes, we here used P. polytes as an experimental model. Using this species, we studied the molecular mechanisms of larval marking formation (Shirataki et al, 2010) and female-specific Batesian mimicry (Iijima et al, 2018(Iijima et al, , 2019; we also recently clarified the wholegenome sequence of this species (Nishikawa et al, 2015), which facilitated analysis of the gene regulation involved in pupal coloration. Furthermore, we established a method of electroporation-mediated gene analysis (Ando and Fujiwara, 2013;Nishikawa et al, 2015) that can provide direct evidence of the functional role of each gene.…”

Section: Introductionmentioning

confidence: 99%

Molecular Mechanisms Underlying Pupal Protective Color Switch in Papilio polytes Butterflies

et al. 2020

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Mimicry is a survival strategy in which organisms deceive their predators by imitating other organisms or the surrounding environment. One example of this involves pupal color polymorphism, which is widely observed in butterflies and moths. It has been suggested that the pupal colors of Papilio butterflies are selected according to the tactile stimulation experienced before pupation (P). Specifically, larvae crawling on smooth leaves become green pupae, but those crawling on rough stems become brown pupae. These protective colors fit with the surrounding environment. However, the detailed molecular mechanisms underlying pupal polymorphism have generally remained unknown. To reveal these mechanisms, we first established control over the green and brown pupal coloration in Papilio polytes under laboratory conditions and clarified temporal and spatial changes of pupal pigments under both conditions. We also analyzed the expression of coloration genes during the pre-pupal stage and at P in the epidermis under the green and brown conditions, by RNA sequencing and quantitative RT-PCR. These analyses revealed that the brown pupal color is regulated mainly by melanin synthesis genes, tyrosine hydroxylase (TH) and laccase 2. In contrast, the green pupal color was suggested to be formed mainly through the expression of both multiple bilin binding protein (BBP)-related genes responsible for blue pigmentation and multiple juvenile hormone binding protein (JHBP)-related genes responsible for yellow pigmentation. Electroporation-mediated RNAi showed that the knockdown of TH or laccase 2 blocked the brown pupal coloration, and that the knockdown of BBP-or JHBP-related genes caused yellow or blue coloration in the green-conditioned pupae, respectively, supporting the above hypothesis. We here report how genes involved in the pupal coloration of P. polytes are regulated, which sheds light on the evolutionary process of pupal protective colors among Lepidoptera.

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Parallel evolution of Batesian mimicry supergene in twoPapiliobutterflies,P. polytesandP. memnon

Abstract: Female-limited polymorphisms underlying Batesian mimicry have evolved independently in two closely related butterfly species.

Cited by 56 publications

References 51 publications

An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

Tissue-specific developmental regulation and isoform usage underlie the role of doublesex in sex differentiation and mimicry in Papilio swallowtails

Molecular Mechanisms Underlying Pupal Protective Color Switch in Papilio polytes Butterflies

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