Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

Sustaining beneficial gut symbioses presents a major challenge for animals, including holometabolous insects. Social insects may meet such challenges through partner fidelity, aided by behavioral symbiont transfer and transgenerational inheritance through colony founders. We address such potential through colony-wide explorations across 13 eusocial, holometabolous insect species in the ant genus Cephalotes. Through amplicon sequencing, we show that previously characterized worker microbiomes are conserved in soldier castes, that adult microbiomes exhibit trends of phylosymbiosis, and that Cephalotes cospeciate with their most abundant adult-enriched symbiont. We find, also, that winged queens harbor worker-like microbiomes prior to colony founding, suggesting vertical inheritance as a means of partner fidelity. Whereas some adult-abundant symbionts colonize larvae, larval gut microbiomes are uniquely characterized by environmental bacteria from the Enterobacteriales, Lactobacillales, and Actinobacteria. Distributions across Cephalotes larvae suggest more than 40 million years of conserved environmental filtering and, thus, a second sustaining mechanism behind an ancient, developmentally partitioned symbiosis.

Automated summary

Social insects maintain beneficial gut symbiosis through behavioral conformity and transgenerational inheritance. A study on 13 eusocial, holometabolous insect species found consistency in worker and soldier microbiomes, phylosymbiosis in adult microbiomes, and cospeciation between Cephalotes ants and the most abundant adult-enriched symbiont. Winged queens have worker-like microbiomes prior to colony founding, indicating vertical inheritance as a means of partner fidelity. Larval gut microbiomes are characterized by environmental bacteria, suggesting over 40 million years of conserved environmental filtering and a second sustaining mechanism behind an ancient, developmentally partitioned symbiosis.