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

Hu, Yi1; D’Amelio, Catherine2; Béchade, Benoît2; Cabuslay, Christian2; Lukasik, Piotr3; Sanders, Jon4; Price, Shauna4; Fanwick, Emily2; Powell, Scott5; Moreau, Corrie4; Russell, Jacob2

Published Apr 28, 2022; Updated Sep 14, 2022 on Dryad. https://doi.org/10.5061/dryad.kwh70rz5d

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Apr 28, 2022 version files 4.89 MB
May 03, 2022 version files 4.89 MB
Sep 14, 2022 version files 60.21 MB

Abstract

Sustaining beneficial gut symbioses presents a major challenge for animals, Including holometabolous insects. Social insects may meet such challenges through behavioral symbiont transfer and transgenerational inheritance through colony founders. We address such potential through colony-wide explorations across 13 eusocial, holometabolous ant species in the genus Cephalotes. Through amplicon sequencing and qPCR, we show that previously characterized worker microbiomes are largely conserved across adult castes, that adult microbiomes exhibit strong trends of phylosymbiosis, and that Cephalotes cospeciate with their most abundant adult symbionts. We find, also, that winged queens harbor worker-like microbiomes prior to colony founding, suggesting that vertical inheritance promotes ancient partner fidelity. While some adult-abundant symbionts colonize guts of larvae, microbiomes from this stage are by environmental bacteria from the Enterobacteriales, Lactobacillales, and Actinobacteria. Re-acquisition of such bacteria, each generation, for >40 million years suggests conserved environmental filtering and, hence, a second mechanism behind distinct symbioses divided by metamorphosis.