Exaptation as a Mechanism for Functional Reinforcement of an Animal Pheromone System

Abstract

Animal sex pheromone systems often exist as multicomponent signals [1-11] to which chemical cues have been added over evolutionary time. Little is known on why and how additional molecules become recruited and conserved in an already functional pheromone system. Here, we investigated the evolutionary trajectory of a series of 15 kDa proteins-termed persuasins-that were co-opted more recently alongside the ancient sodefrin precursor-like factor (SPF) courtship pheromone system in salamanders [9, 12]. Expression, genomic, and molecular phylogenetic analyses show that persuasins originated from a gene that is expressed as a multi-domain protein in internal organs where it has no pheromone function but underwent gene duplication and neofunctionalization. The subsequent evolution combined domain loss and the introduction of a proteolytic cleavage site in the duplicated gene to give rise to two-domain cysteine rich proteins with structural properties similar to SPF pheromones [12]. An expression shift to the pheromone-producing glands, where expression of persuasins was immediately spatiotemporally synchronized with the already available pheromone system, completed the birth of a new pheromone. Electrostatic forces between members of both protein families likely enhance co-localization and simultaneous activation of different female olfactory neurons, explaining why persuasins immediately had a selective advantage. In line with this, behavioral assays show that persuasins increase female receptivity on their own but also exert a cumulative or synergistic effect in combination with SPF, clearly reinforcing the pheromone system as a whole. Our study reveals molecular remodeling of an existing protein architecture as an evolutionary mechanism for functional reinforcement of animal pheromone systems.

A Structural Signature Motif Enlightens the Origin and Diversification of Nuclear Receptors

“…Exaptations are furthermore frequently observed at the gene expression level, mainly through the recruitment of new gene regulatory elements allowing cooptation of gene function in novel organs, tissues or process. This is for example the case of the reinforcement of the courtship pheromone system in frogs via the co-option of the persuasin gene (Maex et al, 2018). This has also been observed in several cases after gene duplication (Force et al, 1999).…”

“…At the molecular level, crystalline lenses first emerged as metabolic enzymes that were later on recruited in the eye for their light-refracting function (Gavelis et al, 2017). More recently, cases of exaptation were identified in the case of retroviral envelope proteins that were recruited as placental proteins in early mammals (Cornelis et al, 2015) or in amphibians as a mechanism for functional reinforcement of a pheromone system (Maex et al, 2018). Exaptations are furthermore frequently observed at the gene expression level, mainly through the recruitment of new gene regulatory elements allowing cooptation of gene function in novel organs, tissues or process.…”

A structural signature motif enlightens the origin and diversification of nuclear receptors

“…Exaptations are furthermore frequently observed at the gene expression level, mainly through the recruitment of new gene regulatory elements allowing cooptation of gene function in novel organs, tissues or process. This is for example the case of the reinforcement of the courtship pheromone system in frogs via the co-option of the persuasin gene [68]. This has also been observed in several cases after gene duplication [69].…”

“…At the molecular level, crystalline lenses first emerged as metabolic enzymes that were later on recruited in the eye for their light-refracting function [66]. More recently, cases of exaptation were identified in the case of retroviral envelope proteins that were recruited as placental proteins in early mammals [67] or in amphibians as a mechanism for functional reinforcement of a pheromone system [68]. Exaptations are furthermore frequently observed at the gene expression level, mainly through the recruitment of new gene regulatory elements allowing cooptation of gene function in novel organs, tissues or process.…”

Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

“…We performed RNA sequencing (RNAseq) of representative salamandrid taxa on a range of Illumina platforms (as specified in Table S2) and at varying sequencing depths, partly in the context of other projects (Stuglik & Babik 2016;Maex et al 2018;Wielstra et al 2019). Specifically for this project, we sequenced eight transcriptomes from 100 mg of tissue per specimen, consisting of combined or separate skin, muscle, or liver samples preserved in RNAlater and frozen at − 80 • C. RNA extraction was performed using standard trizol protocols (for a detailed protocol see Supplementary Methods).…”