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Evolution of Social Insect Polyphenism Facilitated by the Sex Differentiation Cascade.

ABSTRACT: The major transition to eusociality required the evolution of a switch to canalize development into either a reproductive or a helper, the nature of which is currently unknown. Following predictions from the 'theory of facilitated variation', we identify sex differentiation pathways as promising candidates because of their pre-adaptation to regulating development of complex phenotypes. We show that conserved core genes, including the juvenile hormone-sensitive master sex differentiation gene doublesex (dsx) and a krüppel homolog 2 (kr-h2) with putative regulatory function, exhibit both sex and morph-specific expression across life stages in the ant Cardiocondyla obscurior. We hypothesize that genes in the sex differentiation cascade evolved perception of alternative input signals for caste differentiation (i.e. environmental or genetic cues), and that their inherent switch-like and epistatic behavior facilitated signal transfer to downstream targets, thus allowing them to control differential development into morphological castes.

SUBMITTER: Klein A

PROVIDER: S-EPMC4816456 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Evolution of Social Insect Polyphenism Facilitated by the Sex Differentiation Cascade.

Klein Antonia A Schultner Eva E Lowak Helena H Schrader Lukas L Heinze Jürgen J Holman Luke L Oettler Jan J

PLoS genetics 20160331 3

The major transition to eusociality required the evolution of a switch to canalize development into either a reproductive or a helper, the nature of which is currently unknown. Following predictions from the 'theory of facilitated variation', we identify sex differentiation pathways as promising candidates because of their pre-adaptation to regulating development of complex phenotypes. We show that conserved core genes, including the juvenile hormone-sensitive master sex differentiation gene dou ...[more]

PMID: 27031240

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Project description:Rearing conditions may elicit noticeable plastic responses in life-history traits of living organisms. For instance, diet composition has proven to influence prominent traits such as body size, fecundity, and lifespan. In contrast, the social environment may influence the survival rate at immature stages, food consumption, and fat storage. Nevertheless, the physiological mechanisms underlying such responses are largely unknown. In this study, we investigated changes in the proteome of the house cricket Acheta domesticus subjected to diets of different nutritional composition (i.e., protein to carbohydrates ratio) and two distinct social environments (i.e., solitary or in groups). We measured the relative abundances of 685 proteins identified in whole-body cricket samples using high-performance liquid chromatography coupled to tandem mass spectrometry. Differential expression of proteins induced by diet composition and social environment in female and male A. domesticus was assessed in a data-independent proteomics approach. Additionally, we performed a functional analysis of the differentially expressed proteins using comprehensive databases (KEGG and GO). We found that sex alone explained a significant portion (40.87%) of the relative protein abundance variation. Males had a higher representation of proteins involved in metabolic pathways and locomotion. In contrast, females exhibited a higher abundance of proteins related to genetic processes regulation and nutrient catabolism. Moreover, diet composition and social environment induced sex-specific changes in a smaller set of proteins with particular roles. Females had their protein profile affected by diet composition and social environment. The involved proteins were mainly related to several protein synthesis stages, carbohydrate metabolism, and muscle development. In contrast, males were only affected by diet composition, overexpressing proteins related to hormone production, carbohydrate metabolism, and apparently depositing excess protein in the cuticle when fed with a protein-rich diet. It was evident that diet had a more substantial influence on the proteome of the cricket A. domesticus than the social environment, showing that diet composition may exert profound physiological changes in insects in a sex-specific manner.

Project description:Insect ecdysis sequence is composed of pre-ecdysis, ecdysis and post-ecdysis behaviors controlled by a complex cascade of peptide hormones from endocrine Inka cells and neuropeptides in the central nervous system (CNS). Inka cells produce pre-ecdysis and ecdysis triggering hormones (ETH) which activate the ecdysis sequence through receptor-mediated actions on specific neurons in the CNS. Multiple experimental approaches have been used to determine mechanisms of ETH expression and release from Inka cells and its action on the CNS of moths and flies. During the preparatory phase 1-2 days prior to ecdysis, high ecdysteroid levels induce expression of ETH receptors in the CNS and increased ETH production in Inka cells, which coincides with expression of nuclear ecdysone receptor (EcR) and transcription factor cryptocephal (CRC). However, high ecdysteroid levels prevent ETH release from Inka cells. Acquisition of Inka cell competence to release ETH requires decline of ecdysteroid levels and beta-FTZ-F1 expression few hours prior to ecdysis. The behavioral phase is initiated by ETH secretion into the hemolymph, which is controlled by two brain neuropeptides-corazonin and eclosion hormone (EH). Corazonin acts on its receptor in Inka cells to elicit low level ETH secretion and initiation of pre-ecdysis, while EH induces cGMP-mediated ETH depletion and consequent activation of ecdysis. The activation of both behaviors is accomplished by ETH action on central neurons expressing ETH receptors A and B (ETHR-A and B). These neurons produce numerous excitatory or inhibitory neuropeptides which initiate or terminate different phases of the ecdysis sequence. Our data indicate that insect ecdysis is a very complex process characterized by two principal steps: (1) ecdysteroid-induced expression of receptors and transcription factors in the CNS and Inka cells. (2) Release and interaction of Inka cell peptide hormones and multiple central neuropeptides to control consecutive phases of the ecdysis sequence.

Dataset Information

Evolution of Social Insect Polyphenism Facilitated by the Sex Differentiation Cascade.

Publications

Evolution of Social Insect Polyphenism Facilitated by the Sex Differentiation Cascade.

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