Conserved roles of Osiris genes in insect development, polymorphism and protection.

C R Smith,S Pant,M Noureddine,C Morandin

doi:10.1111/jeb.13238

C R Smith, S Pant + Show 2 more

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https://doi.org/10.1111/jeb.13238

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Abstract

Much of the variation among insects is derived from the different ways that chitin has been moulded to form rigid structures, both internal and external. In this study, we identify a highly conserved expression pattern in an insect-only gene family, the Osiris genes, that is essential for development, but also plays a significant role in phenotypic plasticity and in immunity/toxicity responses. The majority of Osiris genes exist in a highly syntenic cluster, and the cluster itself appears to have arisen very early in the evolution of insects. We used developmental gene expression in the fruit fly, Drosophila melanogaster, the bumble bee, Bombus terrestris, the harvester ant, Pogonomyrmex barbatus, and the wood ant, Formica exsecta, to compare patterns of Osiris gene expression both during development and between alternate caste phenotypes in the polymorphic social insects. Developmental gene expression of Osiris genes is highly conserved across species and correlated with gene location and evolutionary history. The social insect castes are highly divergent in pupal Osiris gene expression. Sets of co-expressed genes that include Osiris genes are enriched in gene ontology terms related to chitin/cuticle and peptidase activity. Osiris genes are essential for cuticle formation in both embryos and pupae, and genes co-expressed with Osiris genes affect wing development. Additionally, Osiris genes and those co-expressed seem to play a conserved role in insect toxicology defences and digestion. Given their role in development, plasticity, and protection, we propose that the Osiris genes play a central role in insect adaptive evolution.

Highlights

The chitin-based insect cuticle is a key ingredient in the spectacular ecological and evolutionary success of the insects
Where as a great deal is known about the structure and development of insect cuticle (Wigglesworth, 1957; Andersen, 1979; Hopkins & Kramer, 1992; Merzendorfer, 2011; Tomoyasu & Fujiwara, 2017), some studies using next-generation transcriptomic techniques, such as RNA sequencing (RNAseq), find genes of unknown a 2018 THE AUTHORS
We used a combination of protein BLAST (Altschul et al, 1990) and hidden Markov model searches with HMMER 3.1.2b (Eddy & Wheeler, 2015) using all 24 annotated D. melanogaster Osiris genes

Summary

Introduction

The chitin-based insect cuticle is a key ingredient in the spectacular ecological and evolutionary success of the insects. Chitin forms parts of both the external and internal anatomy of an insect, forming a hard skeleton that has been modified in nearly endless ways and facilitated anatomical, physiological and functional divergence in insect form (Emlen & Nijhout, 2000). Chitin is a barrier to the external environment, and light and flexible enough to form the skeletal basis of locomotary appendages (legs and wings). Where as a great deal is known about the structure and development of insect cuticle (Wigglesworth, 1957; Andersen, 1979; Hopkins & Kramer, 1992; Merzendorfer, 2011; Tomoyasu & Fujiwara, 2017), some studies using next-generation transcriptomic techniques, such as RNA sequencing (RNAseq), find genes of unknown a 2018 THE AUTHORS.

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