Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants

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. diversification ͉ Formicidae ͉ Rhizobiales ͉ symbiosis ͉ trophic level I dentifying the mechanisms underlying adaptation and diversification is a central goal of evolutionary biology. Great strides have been made toward this end through the development of fast and affordable molecular tools, and the joint application of molecular phylogenetics and comparative methods (1-3). One unanticipated theme that has emerged from this work is that bacterial symbionts have played key roles in the evolution and diversification of eukaryotes, starting with endosymbiotic origins of mitochondria and chloroplasts (4). Bacterial symbionts are also prevalent among insects that feed on inaccessible or nutritionally marginal diets such as blood, wood, xylem, and phloem (5). Given the demonstrated nutritional roles of these bacteria, their near-ubiquity in insects that specialize on nutrient-poor diets, their long histories of coevolution, and the diversity of the many groups that harbor nutritional symbionts, it is clear that bacteria have had a strong impact on the dietary evolution and diversification of their insect hosts (6).Symbiosis has played an integral role in the evolution of the ants (Hymenoptera: Formicidae). Throughout the course of their 115-168 million year history (7,8), these diverse and ecologically dominant insects...

Cephaloticoccus gen. nov., a new genus of ‘Verrucomicrobia’ containing two novel species isolated from Cephalotes ant guts

“…Based on the 16S rRNA gene sequence, the isolates shared a sequence similarity of 97.7 % with each other (based on 1552 bp) and a sequence similarity of 91.8 % with their closest cultivated neighbour, Opitutus terrae PB90-1 T (Chin et al, 2001). Additionally, strains CAG34 T and CV41 T shared sequence similarities with their closest environmental clones Fb-17 (obtained from C. rohweri; 99.8 % similarity) and 114a (obtained from C. varians; 99.7 % similarity), respectively (Russell et al, 2009).…”

“…By using PCR amplification and DNA sequencing techniques, previous studies have shown that members of the 'Verrucomicrobia' constitute part of a stable, autochthonous community of symbionts maintained in the guts of Cephalotes 'turtle' ants (Anderson et al, 2012;Kautz et al, 2013;Russell et al, 2009). These symbionts are protected by a proventricular filter (Lanan et al, 2016), remain stable in laboratory-reared colonies and likely coevolved with their hosts (Sanders et al, 2014).…”

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

“…A preliminary assembly of the Wolbachia sequences is hosted on antgenomes.org. The 16S sequence of the γ-proteobacterium showed 98.4% identity with an Enterobacteriaceae of a C. obscurior sample from Florida, USA (voucher RA0330, GenBank: GQ275143), detected during a survey of ant-associated bacteria (Russell et al, 2009).…”

“…The 16S sequence of an unknown Enterobacteriaceae isolated from C. obscurior was previously published (Russell et al, 2009), but the specificity and functionality of this association had not been addressed. Here, we describe it as 'Ca.…”

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

“…Across such a phylogenetic scale, related hosts indeed often harbor similar microbes (see, for example, Jones et al, 2013), as do those with similar diets (Ley et al, 2008). Well documented in the mammals and in several insects, specific symbioses related to particular trophic habits are widely argued to reflect the importance of bacteria in host dietary utilization (see, for example, Ley et al, 2008;Russell et al, 2009). Empirical and metagenomic evidence clearly indicate such an importance (Feldhaar et al, 2007;Douglas, 2009;Muegge et al, 2011).…”