Is the gut microbiota a key driver of social evolution in insects? – MicroSoc

In Task 1, we examined the relationship between gut microbiota and sociality across two life stages.

(1) In the context of family life, we tested whether disrupting gut microbiota affects maternal behaviour. Three hundred females were treated with either a broad-spectrum antibiotic (rifampicin) or water (control). We quantified key maternal behaviours (egg grooming, offspring attendance) and reproductive traits (hatching success, juvenile survival). Gut samples were sequenced (16S rRNA) to confirm the treatment’s impact on microbial composition.

(2) In the context of adult sociality, we analysed aggregation behaviour in 320 field-sampled females, quantified individual gregariousness using video tracking of proximity and activity patterns, and characterised their gut microbiota through 16S rRNA sequencing.

In Task 2, we investigated which social interactions facilitate microbiota transmission. We first tested whether maternal care influences offspring microbiota by manipulating the presence or absence of mothers after hatching and sequencing bacterial communities of mothers and juveniles at different stages. We then examined whether sibling interactions mediate microbiota transfer relevant to juvenile development. Newly hatched juveniles were reared either in isolation or in groups, and their development, survival, and adult behaviour were measured.

Results from Tasks 1 and 2 led us to refine Tasks 3 and 4 to further assess the biological relevance of microbiota in earwig biology. We first attempted to establish axenic lines by bleaching eggs and maintaining juveniles under sterile conditions with antibiotics, then measured the effects on social behaviour, development, and survival. We next tested whether social acquisition of microbiota could explain earwig robustness to chemical pollutants (cadmium). Nine hundred juveniles were reared either alone, with siblings, or with siblings and their mother, and fed cadmium-enriched food at varying doses. Microbiome composition and diversity were analysed after the family phase using 16S rRNA metabarcoding, alongside juvenile fitness measures. Finally, we investigated the existence of a core microbiota in the European earwig by sequencing 90 individuals collected across Europe and North America.

In Task 5, we broadened the project to explore microbial influences on social evolution. This included editing a special issue of an international journal on microbial drivers of sociality across taxa, and writing a review on the social life of the European earwig and the potential role of its microbiota in shaping social interactions.

in progressThe main prediction of MicroSoc was that the gut microbiota plays a key role in regulating social behaviour in the European earwig. The results obtained across the different tasks provided no support for this main prediction. Instead, our experimental studies consistently showed that the microbiota has limited, if any, impact on the biology and sociality of this species. These conclusions are supported by the results of seven studies conducted throughout the project and for which the main results are provided below:

1. Experimental disruption of the gut microbiota in either mothers or juveniles did not influence the expression of maternal care, nor affected any other of the 21 life-history traits measured throughout their life cycle (Van Meyel et al., 2021).

2. Natural variation in aggregation behaviour among adult females was not associated with any specific gut microbiota profile, even though it reflected their overall body condition (Cheutin, Leclerc et al., 2024).

3. The presence of mothers after hatching facilitated the transfer of microbiota to their offspring, and this maternal signature remained detectable several months after mother–offspring interactions ceased (Cheutin, Boucicot et al., 2024).

4. However, preventing the exchange of microbiota between siblings and/or between mothers and juveniles had no effects on offspring development or adult survival (Van Meyel & Meunier, 2022).

5. Removing the external microbiota on the eggs (bleaching) and then rearing the resulting juveniles under axenic (plus antibiotics) conditions profoundly altered their microbiota but did not affect their development, behaviour, or survival (Cheutin, Fontaine et al., in prep.).

6. Exposure to cadmium modified the composition of juvenile microbiota without producing any detectable phenotypic effects (Cheutin, Honorio et al., in press).

7. In line with the lack of a functional microbiota essential for the biology of the European earwig, the microbiota of this species was found to be highly diverse in nature, with substantial variation within and between populations across Europe and North America (Cheutin et al., in prep.).

Together, these findings indicate that the gut microbiota of the European earwig exerts little influence on its social, developmental, and physiological traits. Consequently, the pronounced natural variation in social behaviour observed in this species is unlikely to stem from differences in microbiota composition. Instead, it may reflect other intrinsic or environmental factors that remain to be identified.

More broadly, this limited sensitivity to microbiota alteration may partly explain the remarkable ecological success of the European earwig. Originally native to Europe, this species has now successfully colonised most temperate regions worldwide, suggesting that its biology and social organisation are robust to the substantial microbial and environmental changes associated with global invasion.

The results of the MicroSoc project overall suggest that the European earwig could be one of the few known insect species with a non-functional core microbiota—a surprising and conceptually important finding. In most animals, core microbial communities contribute to key physiological and behavioural functions, including nutrition, immunity, and communication. The apparent absence of such functional dependence in the earwig therefore challenges current assumptions about host–microbe coevolution and opens new avenues for evolutionary and microbiological research.

Future studies should now investigate the evolutionary history of this rare trait. Is the absence of a functional core microbiota unique to F. auricularia, or does it characterise the Dermaptera more broadly? Comparative analyses across related species, coupled with phylogenetic and genomic approaches, could clarify whether this represents a derived loss or an ancestral condition. In parallel, identifying the physiological and molecular mechanisms preventing the establishment or maintenance of a core microbiota will be essential to understand how this insect compensates for functions typically supported by symbionts in other taxa.

Preliminary results from the project also reveal a remarkable diversity in microbiota composition across earwig species. This variation calls for targeted investigations into its ecological and evolutionary drivers, such as diet, habitat, or reproductive mode, as well as into the possible presence of species-specific symbionts. Such studies could help identify whether some Dermaptera have retained mutualistic relationships while others, like F. auricularia, have lost them.

More broadly, although MicroSoc did not provide direct evidence supporting its central prediction—that the gut microbiota drives social evolution in the earwig—its results do not invalidate this hypothesis in other taxa. Insects and vertebrates with more intimate host–microbe dependencies may still exhibit microbiota-mediated social regulation. Thus, the next step is to identify suitable model species in which to test this hypothesis experimentally, ideally those combining social flexibility, tractable microbiota, and ecological relevance.

1. Van Meyel S, Devers S, Dupont S, Dedeine F and Meunier J (2021) Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig. J Evol Biol 34:1034–1045. doi.org/10.1111/jeb.13791

2. Diedermann PHW, Rohlfs M, McMahon DP, Meunier J (2021) Editorial: Microbial Drivers of Sociality – From Multicellularity to Animal Societies. Front Ecol Evol 9:1–4. doi.org/10.3389/fevo.2021.752906

3. Meunier J, Körner M, Kramer J (2022) Parental care. In: Omkar, Mishra G (eds) Reproductive Strategies in Insects. CRC Press, Boca Raton, pp 337–348

A long-standing problem in biology is to understand why and how animal social life has emerged from a solitary state. MicroSoc proposes to address these questions by testing a novel hypothesis positing that social life may not only emerge due to its benefits for the group members but also due to its benefits for their gut microbiota. Using a host species that retains the unique capability to naturally shift between solitary and social life, we will use experimental approaches to identify which gut microbes are associated with host sociality, test how these microbes can benefit from and increase the sociality of their hosts, and shed light on the genetic and chemical mechanisms allowing these gut microbes to induce hosts sociality. We will then take a broader perspective and use an in silico approach to investigate the co-evolutionary history between these microbes and the social life of their hosts across insect species ranging from solitary to complex social systems.