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Feces production as a form of social immunity in an insect with facultative maternal care.

ABSTRACT: BACKGROUND:Social animals have the unique capability of mounting social defenses against pathogens. Over the last decades, social immunity has been extensively studied in species with obligatory and permanent forms of social life. However, its occurrence in less derived social systems and thus its role in the early evolution of group-living remains unclear. Here, we investigated whether lining nests with feces is a form of social immunity against microbial growth in the European earwig Forficula auricularia, an insect with temporary family life and facultative maternal care. RESULTS:Using a total of 415 inhibition zone assays, we showed that earwig feces inhibit the growth of two GRAM+ bacteria, two fungi, but not of a GRAM- bacteria. These inhibitions did not result from the consumed food or the nesting environment. We then demonstrated that the antimicrobial activity against fungus was higher in offspring than maternal feces, but that this difference was absent against bacteria. Finally, we showed that family interactions inhibited the antibacterial activity of maternal feces against one of the two GRAM+ bacteria, whereas it had no effect on the one of nymphal feces. By contrast, antifungal activities of the feces were independent of mother-offspring interactions. CONCLUSION:These results demonstrate that social immunity occurs in a species with simple and facultative social life, and thus shed light on the general importance of this process in the evolution of group-living. These results also emphasize that defecation can be under selection for other life-history traits than simple waste disposal.

SUBMITTER: Diehl JM

PROVIDER: S-EPMC4408575 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Feces production as a form of social immunity in an insect with facultative maternal care.

Diehl Janina M C JM Körner Maximilian M Pietsch Michael M Meunier Joël J

BMC evolutionary biology 20150312

<h4>Background</h4>Social animals have the unique capability of mounting social defenses against pathogens. Over the last decades, social immunity has been extensively studied in species with obligatory and permanent forms of social life. However, its occurrence in less derived social systems and thus its role in the early evolution of group-living remains unclear. Here, we investigated whether lining nests with feces is a form of social immunity against microbial growth in the European earwig F ...[more]

PMID: 25888183

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Project description:Parent-to-offspring transmission of beneficial microorganisms is intimately interwoven with the evolution of social behaviors. Ancestral stages of complex sociality-microbe vectoring interrelationships may be characterized by high costs of intensive parental care and hence only a weak link between the transmission of microbial symbionts and offspring production. We investigate the relationship between yeast symbiont transmission and egg-laying, as well as some general factors thought to drive the "farming" of microscopic fungi by the fruit fly Drosophila melanogaster, an insect with no obvious parental care but which is highly dependent on dietary microbes during offspring development. The process of transmitting microbes involves flies ingesting microbes from their previous environment, storing and vectoring them, and finally depositing them to a new environment. This study revealed that fecal materials of adult flies play a significant role in this process, as they contain viable yeast cells that support larval development. During single patch visits, egg-laying female flies transmitted more yeast cells than non-egg-laying females, suggesting that dietary symbiont transmission is not random, but linked to offspring production. The crop, an extension of the foregut, was identified as an organ capable of storing viable yeast cells during travel between egg-laying sites. However, the amount of yeast in the crop reduced rapidly during periods of starvation. Although females starved for 24 h deposited a smaller amount of yeast than those starved for 6 h, the yeast inoculum produced still promoted the development of larval offspring. The results of these experiments suggest that female Drosophila fruit flies have the ability to store and regulate the transfer of microorganisms beneficial to their offspring via the shedding of fecal material. We argue that our observation may represent an initial evolutionary stage of maternal care through the manipulation of microbial load, from which more specialized feedbacks of sociality and microbe management may evolve.

Dataset Information

Feces production as a form of social immunity in an insect with facultative maternal care.

Publications

Feces production as a form of social immunity in an insect with facultative maternal care.

Similar Datasets

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