Coevolutionary transitions from antagonism to mutualism explained by the Co-Opted Antagonist Hypothesis

Christopher A Johnson,Régis Ferrière,Kelsey Yule,Gordon P Smith,Judith L Bronstein,Goggy Davidowitz

doi:10.1038/s41467-021-23177-x

Abstract

There is now good evidence that many mutualisms evolved from antagonism; why or how, however, remains unclear. We advance the Co-Opted Antagonist (COA) Hypothesis as a general mechanism explaining evolutionary transitions from antagonism to mutualism. COA involves an eco-coevolutionary process whereby natural selection favors co-option of an antagonist to perform a beneficial function and the interacting species coevolve a suite of phenotypic traits that drive the interaction from antagonism to mutualism. To evaluate the COA hypothesis, we present a generalized eco-coevolutionary framework of evolutionary transitions from antagonism to mutualism and develop a data-based, fully ecologically-parameterized model of a small community in which a lepidopteran insect pollinates some of its larval host plant species. More generally, our theory helps to reconcile several major challenges concerning the mechanisms of mutualism evolution, such as how mutualisms evolve without extremely tight host fidelity (vertical transmission) and how ecological context influences evolutionary outcomes, and vice-versa.

Highlights

There is good evidence that many mutualisms evolved from antagonism; why or how, remains unclear
We develop a general eco-coevolutionary framework for investigating the evolutionary transition from antagonism to mutualism and use data-based modeling to advance and evaluate a new hypothesis: the Co-Opted Antagonist (COA) Hypothesis, whereby co-option of an antagonistic species to perform a beneficial function changes the ecology of the interaction and, simultaneously, the interaction evolves to net mutualism
To evaluate the COA hypothesis we develop data-based ecocoevolutionary models for a community in which a lepidopteran insect initially oviposits on, but does not pollinate, its larval host plants, which are pollinated by other species

Summary

Introduction

There is good evidence that many mutualisms evolved from antagonism; why or how, remains unclear. To evaluate the COA hypothesis, we present a generalized eco-coevolutionary framework of evolutionary transitions from antagonism to mutualism and develop a data-based, fully ecologicallyparameterized model of a small community in which a lepidopteran insect pollinates some of its larval host plant species. We develop a general eco-coevolutionary framework for investigating the evolutionary transition from antagonism to mutualism and use data-based modeling to advance and evaluate a new hypothesis: the Co-Opted Antagonist (COA) Hypothesis, whereby co-option of an antagonistic species to perform a beneficial function changes the ecology of the interaction and, simultaneously, the interaction evolves to net mutualism. The evolutionary integration of two consumer-resource interactions, herbivory and nectar-feeding (with pollination as a by-product) may achieve the tight coupling required to induce strong selective pressures on plants (beyond those induced by other pollinators) and the insect This coupling may in turn create the ecological conditions for plant-insect coevolution to drive pollination benefits beyond trophic costs, assimilating the herbivore as a pollinator (either alongside or replacing other pollinators). From the COA hypothesis, we predict that community context, in particular the degree of specialization of the herbivory and nectar-feeding interactions, should influence the transition: generalist larvae that can feed on multiple host plant species may facilitate the transition by ameliorating herbivory costs, whereas generalist adults feeding at multiple nectar sources may hinder the transition by amplifying oviposition costs

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