Can social partnerships influence the microbiome? Insights from ant farmers and their trophobiont mutualists

Abstract

Mutualistic interactions with microbes have played a crucial role in the evolution and ecology of animal hosts. However, it is unclear what factors are most important in influencing particular host–microbe associations. While closely related animal species may have more similar microbiota than distantly related species due to phylogenetic contingencies, social partnerships with other organisms, such as those in which one animal farms another, may also influence an organism's symbiotic microbiome. We studied a mutualistic network of Brachymyrmex and Lasius ants farming several honeydew‐producing Prociphilus aphids and Rhizoecus mealybugs to test whether the mutualistic microbiomes of these interacting insects are primarily correlated with their phylogeny or with their shared social partnerships. Our results confirm a phylogenetic signal in the microbiomes of aphid and mealybug trophobionts, with each species harbouring species‐specific endosymbiont strains of Buchnera (aphids), Tremblaya and Sodalis (mealybugs), and Serratia (both mealybugs and aphids) despite being farmed by the same ants. This is likely explained by strict vertical transmission of trophobiont endosymbionts between generations. In contrast, our results show the ants’ microbiome is possibly shaped by their social partnerships, with ants that farm the same trophobionts also sharing strains of sugar‐processing Acetobacteraceae bacteria, known from other honeydew‐feeding ants and which likely reside extracellularly in the ants’ guts. These ant–microbe associations are arguably more “open” and subject to horizontal transmission or social transmission within ant colonies. These findings suggest that the role of social partnerships in shaping a host's symbiotic microbiome can be variable and is likely dependent on how the microbes are transmitted across generations.

Introduction: The host‐associated microbiome: Pattern, process and function

“…With the exception of a few likely pathogens, aphids and mealybugs harboured only known endosymbionts. The phylogenies for several of their symbionts (Buchnera, Tremblaya and Sodalis) mirrored the host phylogeny, consistent with their strict vertical transmission (Ivens et al, 2018). Such cospeciating symbionts of aphids and mealybugs were rarely found in ants; when they were detected, it was argued to represent "dietary DNA"-that is remnants of symbionts from consumed trophobionts.…”

“…However, in systems ranging from sponges (Thomas et al., ), trees (Kembel et al., ), amphibians (Bletz et al., ) and kelp (Lemay et al., ), host identity is a strong predictor of communities, but the signal disappears at broader phylogenetic levels (e.g., genus and above). Contributions in this issue test the importance of host phylogeny vs. ecology as predictors of microbiome composition by sampling closely related host taxa in controlled environments (Kohl, Dearing, & Bordenstein, ) (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ), related species with contrasting ecologies in uncontrolled, natural environments (Ivens, Gadau, Kiers, & Kronauer, ) and through broad phylogenetic sampling of animals with both divergent and convergent feeding ecologies (Nishida & Ochman, ; Schuelke, Pereira, Hardy, & Bik, ).…”

“…Tendencies towards host specialization could, however, serve as a formidable barrier to such transfer and establishment, a concept that would be supported should symbionts show little overlap among unrelated hosts. To address this, the authors use a rigorous study design with many individuals across different colonies to survey each insect's microbiome (Ivens et al., ). Their efforts across both groups revealed remarkably low‐diversity microbiomes, in keeping with prior findings (e.g., Jing et al., ; Moreau & Rubin, ).…”

“…Ivens and colleagues hence conclude that strong adaptation to disparate hosts presents a very strong barrier to horizontal transfer for endosymbionts. Among the bacteria dominant in their studied ants, Acetobacteraceae were among the most common, with occasional Wolbachia and Oxalobacter (Ivens et al., ). Examinations of correlates across this host group revealed ecology to be a key predictor of the microbiota; that is, Acetobacteraceae are also found in other ants with sugary diets (Russell, Sanders, & Moreau, ) and are predicted to ferment dietary sugars in the gut.…”

“…Examinations of correlates across this host group revealed ecology to be a key predictor of the microbiota; that is, Acetobacteraceae are also found in other ants with sugary diets (Russell, Sanders, & Moreau, ) and are predicted to ferment dietary sugars in the gut. In addition, Lasius species that farm the same mealybugs appear to share the same strains of Acetobacteraceae (Ivens et al., ). While this result awaits further confirmation, it implies that changing ecological conditions (i.e., identities of tended insects) can promote relatively quick changes in the composition of transferrable, extracellular gut symbionts.…”