Abstract

How signal diversity evolves under stabilizing selection in a pheromone-based mate recognition system is a conundrum. Female moths produce two major types of sex pheromones, i.e., long-chain acetates, alcohols and aldehydes (Type I) and polyenic hydrocarbons and epoxides (Type II), along different biosynthetic pathways. Little is known on how male pheromone receptor (PR) genes evolved to perceive the different pheromones. We report the identification of the first PR tuned to Type II pheromones, namely ObruOR1 from the winter moth, Operophtera brumata (Geometridae). ObruOR1 clusters together with previously ligand-unknown orthologues in the PR subfamily for the ancestral Type I pheromones, suggesting that O. brumata did not evolve a new type of PR to match the novel Type II signal but recruited receptors within an existing PR subfamily. AsegOR3, the ObruOR1 orthologue previously cloned from the noctuid Agrotis segetum that has Type I acetate pheromone components, responded significantly to another Type II hydrocarbon, suggesting that a common ancestor with Type I pheromones had receptors for both types of pheromones, a preadaptation for detection of Type II sex pheromone.

Highlights

  • As a case of an efficient, species-specific and well-studied chemical communication system, moth sex pheromone communication has long been a model for the understanding of signaller-receiver evolution

  • We showed that a receptor neuron in sensilla trichodea on the male antennae, responded strongly to the pheromone tetraene 1,3Z,6Z,9Z-19:H

  • These neurons expressed the pheromone receptor gene ObruOR1, which responded to the tetraene when tested in the Xenopus oocyte assay

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Summary

Introduction

As a case of an efficient, species-specific and well-studied chemical communication system, moth sex pheromone communication has long been a model for the understanding of signaller-receiver evolution According to their chemical characteristics, the vast majority of lepidopteran sex pheromones are straight chain, even numbered acetates, aldehydes, and alcohols with 10 to 18 carbon atoms. These so called Type I pheromone components make up the pheromones of around 75% of all moth species for which pheromones have been identified[15]. Type II pheromones consist of polyunsaturated C17-C23 straight-chain, mostly uneven-numbered, skipped conjugated polyenic hydrocarbons and the corresponding epoxide derivatives This type of compounds comprises about 15% of the identified lepidopteran pheromones[15,18,19]. Based on receptor gene characterization, functional studies and phylogenetic analysis we suggest that the receptor for Type II polyene pheromones was recruited from a cluster within the existing PR gene family with previously unknown ligand sensitivities

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