Community analysis of microbial sharing and specialization in a Costa Rican ant-plant-hemipteran symbiosis

Ants have long been renowned for their intimate mutualisms with trophobionts and plants and more recently appreciated for their widespread and diverse interactions with microbes. An open question in symbiosis research is the extent to which environmental influence, including the exchange of microbes between interacting macroorganisms, affects the composition and function of symbiotic microbial communities. Here we approached this question by investigating symbiosis within symbiosis. Ant-plant-hemipteran symbioses are hallmarks of tropical ecosystems that produce persistent close contact among the macroorganism partners, which then have substantial opportunity to exchange symbiotic microbes. We used metabarcoding and quantitative PCR to examine community structure of both bacteria and fungi in a Neotropical ant-plant-scale-insect symbiosis. Both phloem-feeding scale insects and honeydew-feeding ants make use of microbial symbionts to subsist on phloem-derived diets of suboptimal nutritional quality. Among the insects examined here, Cephalotes ants and pseudococcid scale insects had the most specialized bacterial symbionts, whereas Azteca ants appeared to consume or associate with more fungi than bacteria, and coccid scale insects were associated with unusually diverse bacterial communities. Despite these differences, we also identified apparent sharing of microbes among the macro-partners. How microbial exchanges affect the consumer-resource interactions that shape the evolution of ant-plant-hemipteran symbioses is an exciting question that awaits further research.