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. 2018 Nov 27;115(48):12253-12258.
doi: 10.1073/pnas.1719794115. Epub 2018 Nov 12.

Ant-plant Interactions Evolved Through Increasing Interdependence

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Free PMC article

Ant-plant Interactions Evolved Through Increasing Interdependence

Matthew P Nelsen et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Ant-plant interactions are diverse and abundant and include classic models in the study of mutualism and other biotic interactions. By estimating a time-scaled phylogeny of more than 1,700 ant species and a time-scaled phylogeny of more than 10,000 plant genera, we infer when and how interactions between ants and plants evolved and assess their macroevolutionary consequences. We estimate that ant-plant interactions originated in the Mesozoic, when predatory, ground-inhabiting ants first began foraging arboreally. This served as an evolutionary precursor to the use of plant-derived food sources, a dietary transition that likely preceded the evolution of extrafloral nectaries and elaiosomes. Transitions to a strict, plant-derived diet occurred in the Cenozoic, and optimal models of shifts between strict predation and herbivory include omnivory as an intermediate step. Arboreal nesting largely evolved from arboreally foraging lineages relying on a partially or entirely plant-based diet, and was initiated in the Mesozoic, preceding the evolution of domatia. Previous work has suggested enhanced diversification in plants with specialized ant-associated traits, but it appears that for ants, living and feeding on plants does not affect ant diversification. Together, the evidence suggests that ants and plants increasingly relied on one another and incrementally evolved more intricate associations with different macroevolutionary consequences as angiosperms increased their ecological dominance.

Keywords: angiosperms; coevolution; macroevolution; mutualism.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The phylogenetic distribution of ant-associated traits across 10,785 vascular plant genera. Shaded bands behind the phylogeny correspond to geological periods, whereas dashed lines occur at 100-Ma time intervals. The presence (color) or total absence (blank) of species possessing these traits is indicated in rings surrounding the phylogeny. Higher-level taxonomy is plotted for larger clades.
Fig. 2.
Fig. 2.
The evolution of plant-associated traits in ants (solid lines) and the potential to form ant-associated traits in plants (dashed lines) through time. Terminal taxa that possessed a change between the tip and their parent node were not included to facilitate the visualization of earlier transitions. Ant lineages that at least partially fed on plant material or lived arboreally were coded as using plants as a food source and living arboreally. Vertical shading corresponds to geological period.
Fig. 3.
Fig. 3.
Time-scaled ant phylogeny inferred from 1,746 species (1,731 Formicidae), with representatives from 85% of extant ant genera. Branches are shaded by Bayesian analysis of macroevolutionary mixtures-estimated speciation rate. Shaded bands underneath the phylogeny correspond to geological periods, with dashed lines at 50-Ma intervals. Pie charts overlaying nodes indicate the proportional probability of an individual state. Diet, foraging, and nesting location is provided in rings surrounding the tips, with the absence of information on a trait indicated in gray.

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