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Eusociality is linked to caste-specific differences in metabolism, immune system, and somatic maintenance-related processes in an ant species

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Abstract

The social organization of many primate, bird and rodent species and the role of individuals within that organization are associated with specific individual physiological traits. However, this association is perhaps most pronounced in eusocial insects (e.g., termites, ants). In such species, genetically close individuals show significant differences in behavior, physiology, and life expectancy. Studies addressing the metabolic changes according to the social role are still lacking. We aimed at understanding how sociality could influence essential molecular processes in a eusocial insect, the black garden ant (Lasius niger) where queens can live up to ten times longer than workers. Using mass spectrometry-based analysis, we explored the whole metabolome of queens, nest-workers and foraging workers. A former proteomics study done in the same species allowed us to compare the findings of both approaches. Confirming the former results at the proteome level, we showed that queens had fewer metabolites related to immunity. Contrary to our predictions, we did not find any metabolite linked to reproduction in queens. Among the workers, foragers had a metabolic signature reflecting a more stressful environment and a more highly stimulated immune system. We also found that nest-workers had more digestion-related metabolites. Hence, we showed that specific metabolic signatures match specific social roles. Besides, we identified metabolites differently expressed among behavioral castes and involved in nutrient sensing and longevity pathways (e.g., sirtuins, FOXO). The links between such molecular pathways and aging being found in an increasing number of taxa, our results confirm and strengthen their potential universality.

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Data availability

All the data analyzed are available online as electronic supplementary material (ESM1, Tables S1–S7).

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Funding

The study was supported by the CNRS and the French Proteomic Infrastructure (ProFi; ANR-10-INSB-08-03). M. Quque PhD was funded by the University of Strasbourg and the French Ministry of Education, Research and Innovation.

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  1. Fabrice Bertile and Dimitri Heintz share co-seniorship of the paper.

Authors and Affiliations

  1. Université de Strasbourg, CNRS, IPHC UMR 7178, 23 rue du Loess, F-67000, Strasbourg, France

    Martin Quque, François Criscuolo, Cédric Sueur & Fabrice Bertile

  2. Plant Imaging and Mass Spectrometry (PIMS), Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, 12 rue du Général Zimmer, F-67000, Strasbourg, France

    Claire Villette & Dimitri Heintz

  3. Institut Universitaire de France, 75005, Paris, France

    Cédric Sueur

  4. Infrastructure Nationale de Protéomique ProFI, FR2048, Strasbourg, France

    Fabrice Bertile

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  1. Martin Quque
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Contributions

DH, FB, FC, CS and MQ designed the experimental protocol, MQ performed the behavioral observations and prepared samples before use in omics; DH prepared samples for metabolomics and performed the raw data processing; CV performed the LC-HRMS injections for metabolomics; MQ performed the whole statistical analysis and looked for manual functional annotation of metabolites; FB retrieved KEGG functional information; MQ wrote the first draft; CV and DH wrote methodological parts related to metabolomics of this draft; all authors edited the first draft.

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Correspondence to Martin Quque.

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Quque, M., Villette, C., Criscuolo, F. et al. Eusociality is linked to caste-specific differences in metabolism, immune system, and somatic maintenance-related processes in an ant species. Cell. Mol. Life Sci. 79, 29 (2022). https://doi.org/10.1007/s00018-021-04024-0

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