Impact of animal socioecology on gut microbial communities : insights from wild meerkats in the Kalahari

Abstract

1. The social organisation of animals likely shapes the composition, diversity and stability of microbiomes, giving rise to the concept of the 'social microbiome'-microbial communities shared within and across social units, or 'islands', ranging from individuals to entire ecosystems. Understanding the connections and their underlying drivers is crucial for revealing how socioecology influences microbiomes and associated health outcomes. However, empirical assessments are still limited, and the relative influence of social organisation compared to intrinsic (biological) and extrinsic (environmental) factors in shaping microbiomes is particularly unclear. 2. Here, we used a long-term, individual-based study of Kalahari meerkats (Suricata suricatta) to test predictions from the social microbiome concept. We assessed the relative influence of social factors, biological traits and environmental variables on gut microbial communities, while also accounting for the effects of microbial phylogenetic relatedness and within-host associations or co-occurrence independent of phylogeny. 3. Meerkat microbiomes exhibited highly 'nested' and weakly 'modular' structures: individuals with lower diversity hosted amplicon sequence variants (ASVs) that were subsets of the overall community, though some bacterial taxa clustered distinctly among hosts. Microbiomes were more similar within social groups than between them. 4. Group membership strongly influenced the co-occurrence of many beneficial ASVs, as well as a few potentially harmful ones. This effect was stronger than that of kinship, though closer relatives shared more similar microbiomes within some groups. While a range of social, biological and environmental factors influenced bacterial abundance, group membership, individual age and sampling time since sunrise had the most significant impact. ASV-ASV co-occurrence within hosts, independent of phylogeny, also played a major role. In contrast, individual-level social traits (e.g. dominance, immigration), other environmental (e.g. sampling temperature, rainfall, hours since foraging), demographic (sex) and health-related factors (body condition, disease status) had weaker effects on bacterial abundance. 5. We show that gut microbiomes are shaped by a combination of factors, highlighting the importance of separating the effects of social organisation from individual social traits, biological factors, environmental influences and microbe-microbe interactions. By identifying drivers of both beneficial and detrimental bacterial co-occurrence, we provide a foundation for assessing how the social microbiome affects animal health and fitness.