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Caste-specific RNA editomes in the leaf-cutting ant Acromyrmex echinatior

ABSTRACT: Eusocial insects have evolved the capacity to generate adults with distinct morphological, reproductive and behavioural phenotypes from the same genome. Recent studies suggest that RNA editing might enhance the diversity of gene products at the post-transcriptional level, particularly to induce functional changes in the nervous system. Using head samples from the leaf-cutting ant Acromyrmex echinatior, we compare RNA editomes across eusocial castes, identifying ca. 11,000 RNA editing sites in gynes, large workers and small workers. Those editing sites map to 800 genes functionally enriched for neurotransmission, circadian rhythm, temperature response, RNA splicing and carboxylic acid biosynthesis. Most A. echinatior editing sites are species specific, but 8–23% are conserved across ant subfamilies and likely to have been important for the evolution of eusociality in ants. The level of editing varies for the same site between castes, suggesting that RNA editing might be a general mechanism that shapes caste behaviour in ants.

ORGANISM(S): Acromyrmex echinatior

PROVIDER: GSE51576 | GEO | 2014/10/02

SECONDARY ACCESSION(S): PRJNA223531

REPOSITORIES: GEO

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Project description:Background: Eusociality is widely considered to evolve through kin selection, where the reproductive success of an individual’s close relative is favored at the expense of its own. High genetic relatedness is thus considered a prerequisite for eusociality. While ants are textbook examples of eusocial animals, not all ants form colonies of closely related individuals. One such example is the ectatommine ant Rhytidoponera metallica, which predominantly forms predominantly queen-less colonies that have such a low intra-colony relatedness that they have been proposed to represent a transient, unstable form of eusociality. However, R. metallica is among the most abundant and widespread ants on the Australian continent. This apparent contrast provides an example of how inclusive fitness may not by itself explain the maintenance of eusociality and raises the question of what other selective advantages maintain their eusocial lifestyle. Results: We provide a comprehensive portrait of the venom of R. metallica and show that the colony-wide venom consists of a, for an ant, exceptionally high diversity of functionally distinct toxins. These toxins have evolved under strong positive selection, which is normally expected to reduce genetic variance. Yet, R. metallica exhibits remarkable intra-colony variation, with workers sharing only a relatively small proportion of toxins in their venoms. We also find that this variation is not due to the presence of chemical castes, but that it has a genetic foundation that is at least in part explained by toxin allelic diversity. Conclusions: Taken together, our results suggest that the toxin diversity contained in R. metallica colonies may be maintained by a form of group selection, which selects for colonies that can exploit more resources and defend against a wider range of predators. We propose that increased intra-colony genetic variance resulting from low kinship may itself provide a selective advantage in the form of an expanded pharmacological venom repertoire. These findings provide an example of how group selection on adaptive phenotypes may contribute to maintaining eusociality where a prerequisite for kin selection is diminished.

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Caste-specific RNA editomes in the leaf-cutting ant Acromyrmex echinatior

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