Abstract

Insect chemical communication and chemosensory systems rely on proteins coded by several gene families. Here, we have combined protein modeling with evolutionary analysis in order to study the evolution and structure of chemosensory proteins (CSPs) within arthropods and, more specifically, in ants by using the data available from sequenced genomes. Ants and other social insects are especially interesting model systems for the study of chemosensation, as they communicate in a highly complex social context and much of their communication relies on chemicals. Our ant protein models show how this complexity has shaped CSP evolution; the proteins are highly modifiable by their size, surface charge and binding pocket. Based on these findings, we divide ant CSPs into three groups: typical insect CSPs, an ancient 5-helical CSP and hymenopteran CSPs with a small binding pocket, and suggest that these groups likely serve different functions. The hymenopteran CSPs have duplicated repeatedly in individual ant lineages. In these CSPs, positive selection has driven surface charge changes, an observation which has possible implications for the interaction between CSPs and ligands or odorant receptors. Our phylogenetic analysis shows that within the Arthropoda the only highly conserved gene is the ancient 5-helical CSP, which is likely involved in an essential ubiquitous function rather than chemosensation. During insect evolution, the 6-helical CSPs have diverged and perform chemosensory functions among others. Our results contribute to the general knowledge of the structural differences between proteins underlying chemosensation and highlight those protein properties which have been affected by adaptive evolution.

Highlights

  • Chemical communication is crucial for insects, as their perception of the world is dominated by odors

  • We modeled the seven orthologous ant chemosensory proteins (CSPs) (CSP1-7) (Figure 1)

  • Our ant examples show that CSP proteins have extensive size, charge and binding pocket variation that can presumably be linked to their interaction with odorant receptors (OR) or ligands

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Summary

Introduction

Chemical communication is crucial for insects, as their perception of the world is dominated by odors. Most of their behavior from courtship and mating to locating resources such as food and a suitable habitat are dependent on chemical senses. The reception of chemical messages in insects starts when specific carrier proteins, such as the odorant binding proteins (OBP) or chemosensory proteins (CSP), bind and solubilize odorants and pheromones and transport them through the aqueous hemolymph [2,3]. The chemical messages carried by the OBPs and CSPs are decoded when odorant receptors (OR), or in some cases gustatory receptors (GR), selectively bind the chemicals [4]. Chemosensory gene families have been intensively studied in the context of gene family dynamics and they usually show birth-and-death evolution with purifying selection being the main force [5,6,7]

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