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Using text-mined trait data to test for cooperate-and-radiate co-evolution between ants and plants

Kaur, KM; Male, PJG; Spence, E; Gomez, C; Frederickson, ME

PLOS COMPUTATIONAL BIOLOGY
2019
VL / 15 - BP / - EP /
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. Author summary Many plants and animals depend on other species for nutrition, protection, or dispersal, a type of ecological interaction known as mutualism. Mutualisms often help organisms thrive in new or harsh environments, thereby increasing their ecological success. We studied whether mutualism also increases evolutionary success by affecting lineage diversification, or the net result of the formation and loss of species over evolutionary time (i.e., speciation minus extinction). We focused on the widespread mutualism between ants and plants, in which ants act as protective 'bodyguards' or seed dispersers for plants and gain food or shelter in return. Previous research has found that the evolution of ant-plant mutualisms increased plant diversification. Here, we asked whether the same is true for ant diversification. We used a novel, automated approach to gather trait data from the abstracts of over 89,000 scientific articles about ants, and identified 432 mutualistic ant species and 2,909 non-mutualistic ant species. We then used this trait information to model how mutualism has evolved and influenced diversification across a recent ant phylogeny. Our analysis suggests that instead of causally enhancing diversification, mutualism evolves more often in lineages that are already diversifying quickly and then slows ant diversification.

AccesS level

DOAJ Gold, Green Published

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PROYECTO FINANCIADO POR PLAN NACIONAL DE INVESTIGACIÓN AGENCIA ESTATAL DE INVESTIGACIÓN, MINISTERIO DE CIENCIA E INNOVACIÓN. PID2019-109127RB-I00