Group recognition in the German cockroach, a subsocial omnivore, is based on faecal odour preference that is modulated by coprophagy, diet and learning

Abstract

Faecal odours attract cockroaches to aggregations, where conspecific faeces provide nutrients and seed the gut microbiota. Because these odours arise from the gut and faecal microbial communities, which are shaped by coprophagy and diet, discrete aggregations within a heterogeneous landscape can produce distinct faecal odour profiles. How such odour diversity influences recognition, group affiliation and ultimately aggregation remains unclear. We manipulated coprophagy and then diet quality in gnotobiotic nymphs to generate groups with distinct faecal odour signatures, then raised them to the adult stage and collected their faeces for behavioural assays. Naive nymphs lacking coprophagy experience were equally attracted to faecal odours from all treatment groups, suggesting an innate attraction to conspecific faeces. By contrast, experienced nymphs preferred the faecal odour of their natal group over foreign groups, suggesting learned group-specific recognition. In associative learning assays pairing a faecal odour with a glucose reward, nymphs preferentially aggregated with the conditioned odour over novel odours. These results show that aggregation in neonate cockroaches is mediated by both an innate attraction to conspecific faecal odour and learned preferences for specific odourants encountered during coprophagy soon after they hatch. We propose that these mechanisms guide neonates towards natal aggregations, facilitating acquisition of a locally adapted gut microbial community.