The role of symbiotic bacteria in the evolution of ant herbivory

Yi Hu

doi:10.17918/etd-7064

Ants are one of the world's most dominant and diverse animal groups with nearly unrivaled biomass. It has been long argued that one key to their evolutionary success has been their use of liquid diets, and several major taxa have been shown to rely heavily on exudates from plants or insects. As stable isotope analyses suggest that many ants from tropical rainforest canopies exhibit trophic overlap with herbivorous insects, it has been argued that these ants' diets may largely consist of nitrogen-poor exudates. These findings led researchers to hypothesize that "herbivorous" ants rely on the contributions of nutritional bacterial symbionts to overcome the suspected low quality of their diets. In order to test this hypothesis, I first examined whether herbivorous ants have a great degree of bacterial community stability. Through comprehensively characterizing the complex symbiotic gut communities of the herbivorous ant Cephalotes varians across individuals, colonies and geographic regions, I found that C. varians bacterial communities were dominated by 16 core species which hailed from ant-specific clades containing relatives from other Cephalotes species. In spite of this stability, the relative abundance and genotypic composition of C. varians core species varied across colonies, suggesting symbiotic variability as a potential source of heritable, adaptive variation. I further applied both experimental and metagenomic approaches to assess symbiont-mediated roles in nitrogen provisioning for Cephalotes varians. Experimental measures of nutritional contributions to nitrogen recycling demonstrated that gut symbionts of C. varians incorporate nitrogen from urea into amino acids for their host ants. Metagenomic analyses confirmed the symbionts' contribution to host nutrition through recycling of nitrogenous wastes and biosynthesis of amino acids. Unlike obligate bacteriocyte-dwelling symbionts, nitrogen provisioning in the Cephalotes system involves both essential and non-essential amino acids, with key steps of nitrogen metabolic pathways being shared among several extracellular gut symbionts. These findings provide the second line evidence for nutritional contributions by symbiotic bacteria of herbivorous ants, adding strong support to the hypothesis that symbionts have a major role in the success of arboreal ant herbivores. While considerable evidence suggests convergent associations between herbivorous ants and particular symbiotic microbes, little is known about the mode and timing of microbial shifts in the relation to shifts in host diets. To address this question, I focused on Argentine ants (Linepithema humile), which have undergone a very recent shift toward reliance on sugar-rich and nitrogen-poor honeydew diets. Through comparing the bacterial communities between ants from native and introduced populations and examining bacterial communities of an introduced population across multiple years in Rice Canyon, CA. I found no evidence for a major shift in symbioses in association with Argentine ants' invasion into the southwestern United States and no changes in the microbiota during a multi-year period of trophic reduction in Rice Canyon. Combined with low bacterial abundance across most Argentine ants, my findings argue against a major role for bacteria as drivers of the Argentine ants' invasive trophic shift. Taken together, the results from this dissertation suggest that bacterial symbionts may not have been essential precursors for the shifts to herbivory throughout the history of the ants, but instead play an important role in the maintenance and success of ant herbivory over broader evolutionary timescales.

The role of symbiotic bacteria in the evolution of ant herbivory

Files and links (1)

Abstract

Metrics

Details

The role of symbiotic bacteria in the evolution of ant herbivory

Files and links (1)

Abstract

Metrics

Details

Drexel University Social media