Review Article

Hotspots for symbiosis: function, evolution, and specificity of ant-microbe associations from trunk to tips of the ant phylogeny (Hymenoptera: Formicidae)

Russell, J.A., Sanders, J.G. & Moreau, C.S.


Abstract: Ants are among the world's most abundant and dominant non-human animals. Yet in spite of our growing knowledge of microbes as important associates of many animals, we have only begun to develop a broad understanding of the ants' microbial symbionts and their impacts across this diverse family (Hymenoptera: Formicidae). With an impressive degree of niche diversification across their ~ 140 million year history, evolution has performed a range of natural experiments among the ants, allowing studies of symbiosis through a lens of comparative biology. Through this lens it is gradually becoming clear that specialized symbioses can be gained or lost in conjunction with important shifts in ant biology, ranging from dietary ecology to investment in chemical defense. Viewing symbiosis across the ant phylogeny has also lent an additional insight – that the presence of specialized and ancient microbial symbionts is a patchily distributed attribute of ant biology. In fact, recent evidence suggests that several groups of ants harbor very few microbial symbionts – at least those of a eubacterial nature. These combined findings raise the possibility that the importance of symbiosis has fluctuated throughout the evolutionary history of the ants, making "hotspot" lineages stand out amongst potential symbiotic coldspots. In this review, we discuss these phenomena, highlighting the evidence for symbiont turnover and symbiotic hotspots that has accumulated largely over the past decade. We also emphasize the types of bacteria and fungi that can be found more sporadically across a range of ants, even beyond apparent hotspot taxa. An emerging theme from the literature suggests that several ant-enriched or ant-specific microbial lineages are common associates of farflung hosts from across this insect family, suggesting that a recurring symbiotic menagerie has sojourned across the ants for quite some time. In summary, the weight of the evidence suggests the importance of symbiosis across several ant taxa, supporting a growing appreciation for the major role of symbiosis in animal biology. Yet apparently low-density bacterial communities in some ants raise questions about symbiont ubiquity and the forces governing the microbial populations that colonize these hosts and the world's many eukaryotes beyond.