Abstract

Mutualisms may be “key innovations” that spur lineage diversification by augmenting niche breadth, geographic range, or population size, thereby increasing speciation rates or decreasing extinction rates. Whether mutualism accelerates diversification in both interacting lineages is an open question. Research suggests that plants that attract ant mutualists have higher diversification rates than non-ant associated lineages. We ask whether the reciprocal is true: does the interaction between ants and plants also accelerate diversification in ants, i.e. do ants and plants cooperate-and-radiate? We used a novel text-mining approach to determine which ant species associate with plants in defensive or seed dispersal mutualisms. We investigated patterns of lineage diversification across a recent ant phylogeny using BiSSE, BAMM, and HiSSE models. Ants that associate mutualistically with plants had elevated diversification rates compared to non-mutualistic ants in the BiSSE model, with a similar trend in BAMM, suggesting ants and plants cooperate-and-radiate. However, the best-fitting model was a HiSSE model with a hidden state, meaning that diversification models that do not account for unmeasured traits are inappropriate to assess the relationship between mutualism and ant diversification. Against a backdrop of diversification rate heterogeneity, the best-fitting HiSSE model found that mutualism actually decreases diversification: mutualism evolved much more frequently in rapidly diversifying ant lineages, but then subsequently slowed diversification. Thus, it appears that ant lineages first radiated, then cooperated with plants.

Highlights

  • How have species interactions contributed to the diversification of life on Earth? Ehrlich and Raven [1] famously proposed escape-and-radiate co-evolution as an engine of plant and insect diversification

  • Many plants and animals depend on other species for nutrition, protection, or dispersal, a type of ecological interaction known as mutualism

  • The textmining identified 129 ant species in 39 genera as seed dispersers, compared to 268 ant species in 60 genera in the hand-compiled dataset, meaning that 44 ant species were in the text-mining results only, and 183 species were in the hand-compiled dataset only

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Summary

Introduction

How have species interactions contributed to the diversification of life on Earth? Ehrlich and Raven [1] famously proposed escape-and-radiate co-evolution as an engine of plant and insect diversification. Recent studies have linked mutualism evolution to accelerated lineage diversification [2,3,4], suggesting that mutualism either buffers lineages against extinction, promotes speciation as lineages enter new adaptive zones, or both [5]. Building on previous research showing that partnering with ants enhances plant diversification [3,4], we ask if interacting mutualistically with plants enhances ant diversification. Mutualism theory generally predicts the opposite; mutualism is expected to hinder diversification [6,7] because the interdependence of partners, conflicts of interest between them, or the invasion of selfish “cheaters” should make mutualistic lineages vulnerable to extinction [8,9,10]. Recent studies show that mutualism can expand a lineage’s realized niche [11,12], potentially creating ecological opportunity

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