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Bacterial Gut Symbionts Are Tightly Linked With the Evolution of Herbivory in Ants

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Bacterial Gut Symbionts Are Tightly Linked With the Evolution of Herbivory in Ants

Jacob A Russell et al. Proc Natl Acad Sci U S A.

Abstract

Ants are a dominant feature of terrestrial ecosystems, yet we know little about the forces that drive their evolution. Recent findings illustrate that their diets range from herbivorous to predaceous, with "herbivores" feeding primarily on exudates from plants and sap-feeding insects. Persistence on these nitrogen-poor food sources raises the question of how ants obtain sufficient nutrition. To investigate the potential role of symbiotic microbes, we have surveyed 283 species from 18 of the 21 ant subfamilies using molecular techniques. Our findings uncovered a wealth of bacteria from across the ants. Notable among the surveyed hosts were herbivorous "turtle ants" from the related genera Cephalotes and Procryptocerus (tribe Cephalotini). These commonly harbored bacteria from ant-specific clades within the Burkholderiales, Pseudomonadales, Rhizobiales, Verrucomicrobiales, and Xanthomonadales, and studies of lab-reared Cephalotes varians characterized these microbes as symbiotic residents of ant guts. Although most of these symbionts were confined to turtle ants, bacteria from an ant-specific clade of Rhizobiales were more broadly distributed. Statistical analyses revealed a strong relationship between herbivory and the prevalence of Rhizobiales gut symbionts within ant genera. Furthermore, a consideration of the ant phylogeny identified at least five independent origins of symbioses between herbivorous ants and related Rhizobiales. Combined with previous findings and the potential for symbiotic nitrogen fixation, our results strongly support the hypothesis that bacteria have facilitated convergent evolution of herbivory across the ants, further implicating symbiosis as a major force in ant evolution.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
16S rRNA phylogeny of ant-associated Rhizobiales symbionts and their GenBank relatives. Tree topology was obtained through a maximum-likelihood analysis, and statistical support from each of three separate analyses is indicated at each node: Bootstrap values for nodes with ≥80% support are indicated above (likelihood) and below (parsimony) the branches leading to their respective nodes; posterior probabilities ≥90% from Bayesian analyses are similarly indicated using black circles. Ant-associates are presented in red font and named after their hosts; those identified in previous studies are presented with underlined font. In several instances, collection or clone IDs are included to help distinguish between similarly named associates. Bacteria from plants and other animals are presented in purple and orange fonts, respectively, whereas those from other or unspecified habitats are in black. GenBank accession numbers and full sequence names for taxa in this tree are presented in Table S6. Photo inset by C. S. Moreau. Outgroups Wolbachia and P. aeruginosa are not pictured.
Fig. 2.
Fig. 2.
Rhizobiales bacteria are prevalent in herbivorous ants. Average trophic position (δ15Nant − δ15Nplant; ‰) is plotted against the frequency of Rhizobiales gut bacteria in 47 ant genera (values calculated from data in refs. 30, 31). Sample sizes (maximum number of species) for all genera harboring Rhizobiales are provided next to their respective data points. Genera highlighted in green represent those whose standardized nitrogen isotope values overlapped with those of known arthropod herbivores (e.g., δ15Nherbivore − δ15Nplant ≤ 3.76); the standardized stable isotope values for genera highlighted in yellow overlapped with those of known arthropod predators (δ15Npredator − δ15Nplant ≥ 3.99; values calculated from ref. ; SI). Data points corresponding to Rhizobiales-harboring ant genera (i.e., those with nonzero values on the y axis) are, from left to right, Cephalotes, Tetraponera, Dolichoderus, Cataulacus, Tetramorium, and Pheidole.
Fig. 3.
Fig. 3.
Rhizobiales distributions reveal independent origins within herbivorous taxa. Phylogeny (pruned from ref. 8) depicts relatedness among the ant genera included in our analyses of Rhizobiales prevalence vs. trophic position. Within the adjacent table we have included: (i) frequency of Rhizobiales; (ii) trophic level (i.e., average δ15Nant − δ15Nplant); and (iii) taxonomic classification for each genus. Green and yellow shading identify herbivorous and predatory genera, respectively, as described for Fig. 2. The single genus without a highlight (i.e., Pristomyrmex) did not show overlap with either trophic level. Taxa presented in red font were hosts of Rhizobiales bacteria. The placement of Paratrechina (gray branch) is based on analyses by C. S. Moreau.

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