The evolution of abdominal microbiomes in fungus‐growing ants

Abstract

The attine ants are a monophyletic lineage that switched to fungus farming ca. 55–60 MYA. They have become a model for the study of complex symbioses after additional fungal and bacterial symbionts were discovered, but their abdominal endosymbiotic bacteria remain largely unknown. Here, we present a comparative microbiome analysis of endosymbiotic bacteria spanning the entire phylogenetic tree. We show that, across 17 representative sympatric species from eight genera sampled in Panama, abdominal microbiomes are dominated by Mollicutes, α‐ and γ‐Proteobacteria, and Actinobacteria. Bacterial abundances increase from basal to crown branches in the phylogeny reflecting a shift towards putative specialized and abundant abdominal microbiota after the ants domesticated gongylidia‐bearing cultivars, but before the origin of industrial‐scale farming based on leaf‐cutting herbivory. This transition coincided with the ancestral single colonization event of Central/North America ca. 20 MYA, documented in a recent phylogenomic study showing that almost the entire crown group of the higher attine ants, including the leaf‐cutting ants, evolved there and not in South America. Several bacterial species are located in gut tissues or abdominal organs of the evolutionarily derived, but not the basal attine ants. The composition of abdominal microbiomes appears to be affected by the presence/absence of defensive antibiotic‐producing actinobacterial biofilms on the worker ants' cuticle, but the significance of this association remains unclear. The patterns of diversity, abundance and sensitivity of the abdominal microbiomes that we obtained explore novel territory in the comparative analysis of attine fungus farming symbioses and raise new questions for further in‐depth research.

Synergies Between Division of Labor and Gut Microbiomes of Social Insects

“…Host transmission of heritable extracellular symbionts has been hypothesized to result in long-term associations between some social insects and specialized microbiota. Termites, social corbiculate bees, and clades of ants consistently host microbial phylotypes over evolutionary timescales, as indicated by patterns of phylogenetic congruence of microbial communities with hosts (Russell et al, 2009;Dietrich et al, 2014;Sanders et al, 2014;Kwong et al, 2017;Lukasik et al, 2017;Bourguignon et al, 2018;Sapountzis et al, 2019). Although this indicates vertical transmission across generations, most symbioses are characterized by the presence of at least some degree of host switching, suggesting that horizontal transmission persists across host clades (Koch et al, 2013;Sanders et al, 2014;Kwong et al, 2017;Bourguignon et al, 2018).…”

Evolutionary “Experiments” in Symbiosis: The Study of Model Animals Provides Insights into the Mechanisms Underlying the Diversity of Host–Microbe Interactions

“…[79] Since in addition to the mutualistic fungus they cultivate for food, fungus-growing ants harbor complex microbiomes, [80,81] they represent a good model for understanding a multilayered symbiosis. For example, fungus-growing ants of the genus Atta, form a symbiosis with fungi that they cultivate as the main food source for the colony.…”

“…For example, fungus-growing ants of the genus Atta, form a symbiosis with fungi that they cultivate as the main food source for the colony. [79] Since in addition to the mutualistic fungus they cultivate for food, fungus-growing ants harbor complex microbiomes, [80,81] they represent a good model for understanding a multilayered symbiosis. Also, studies in the African turquoise killifish Nothobranchius furzeri, one of the shortest lived vertebrate species, revealed that the gut microbiota plays a key role in modulating life span [82] (see also Finlay et al [83] in this issue).…”

Convergence, constraint and the potential for mutualism between ants and gut microbes

“…Nevertheless, the correspondence between gut bacteria and historical biogeography suggests that strong constraints on the assembly of attine gut bacterial communities are also at play. As Sapountzis et al () note, future studies of higher‐attine lineages that independently recolonized South America will clarify the extent of the geographic and phylogenetic nature of these constraints. Moreover, although the higher attines that diversified in Middle America have higher gut bacterial densities than do other attines, even these species appear to have fewer gut bacteria than other, non‐attine ants whose gut bacteria confer known nutritional benefits (Rubin, Kautz, Wray, & Moreau, ; Sanders et al ).…”

“…Sapountzis, Nash, Schiøtt, and Boomsma () go inside the ants themselves to examine gut bacterial communities across 17 attine species, representing the major transitions in fungal agriculture. Comparing attines across dietary transitions, they find some evidence for increased bacterial densities and reduced bacterial diversity in ant guts and associated abdominal material with increased dietary specialization, consistent with a concomitant shift towards a more specialized gut bacterial community (Figure ).…”