Cycad-Weevil Pollination Symbiosis Is Characterized by Rapidly Evolving and Highly Specific Plant-Insect Chemical Communication.

Shayla Salzman,Damon Crook,Michael Calonje,Dennis W Stevenson,Naomi E Pierce,Robin Hopkins

doi:10.3389/fpls.2021.639368

Abstract

Coevolution between plants and insects is thought to be responsible for generating biodiversity. Extensive research has focused largely on antagonistic herbivorous relationships, but mutualistic pollination systems also likely contribute to diversification. Here we describe an example of chemically-mediated mutualistic species interactions affecting trait evolution and lineage diversification. We show that volatile compounds produced by closely related species of Zamia cycads are more strikingly different from each other than are other phenotypic characters, and that two distantly related pollinating weevil species have specialized responses only to volatiles from their specific host Zamia species. Plant transcriptomes show that approximately a fifth of genes related to volatile production are evolving under positive selection, but we find no differences in the relative proportion of genes under positive selection in different categories. The importance of phenotypic divergence coupled with chemical communication for the maintenance of this obligate mutualism highlights chemical signaling as a key mechanism of coevolution between cycads and their weevil pollinators.

Highlights

Obligate mutualistic associations involving a high degree of specialization by both partners such as those between figs and fig wasps and yuccas and yucca moths are less common in nature, and yet the analysis of such systems is vital to our understanding of mechanisms underlying the evolution of plant/insect interactions (Pellmyr, 2003; Herre et al, 2008)
Using insect physiology and behavior, we demonstrate that plant-insect chemical communication and push-pull pollination is consistent across these two species pairs and is driving the relationship of the Rhopalotria/Zamia mutualism
We identify the chemical communication underlying the R. slossoni/Z. integrifolia mutualism and find the push-pull mechanism to match that demonstrated in R. furfuracea/Z. furfuracea (Salzman et al, 2020) in which weevils have specialized to perceive only the signal emitted by their respective host plant

Summary

Introduction

Obligate mutualistic associations involving a high degree of specialization by both partners such as those between figs and fig wasps and yuccas and yucca moths are less common in nature, and yet the analysis of such systems is vital to our understanding of mechanisms underlying the evolution of plant/insect interactions (Pellmyr, 2003; Herre et al, 2008) Studies of these and other pollination systems (Holland and Fleming, 1999; Kawakita, 2010) have highlighted morphological and behavioral traits associated with mutualism, and begun to identify mechanisms of diversification and speciation associated with these lineages (Althoff et al, 2012; Hembry et al, 2013; Suinyuy et al, 2015). We are interested in identifying: (1) traits driving these relationships, (2) whether these traits are diverging across closely related taxa, and (3) the role of selection in trait divergence Zamia cycads and their Rhopalotria pollination mutualists are an ideal study system as they represent an understudied obligate brood-site pollination mutualism where the importance of volatile signaling is clear

Methods

Results

Conclusion