Social behaviour and gut microbiota in red‐bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality

Abstract

Vertebrate gut microbiota form a key component of immunity and a dynamic link between an individual and the ecosystem. Microbiota might play a role in social systems as well, because microbes are transmitted during social contact and can affect host behaviour. Combining methods from behavioural and molecular research, we describe the relationship between social dynamics and gut microbiota of a group-living cooperative species of primate, the red-bellied lemur (Eulemur rubriventer). Specifically, we ask whether patterns of social contact (group membership, group size, position in social network, individual sociality) are associated with patterns of gut microbial composition (diversity and similarity) between individuals and across time. Red-bellied lemurs were found to have gut microbiota with slight temporal fluctuations and strong social group-specific composition. Contrary to expectations, individual sociality was negatively associated with gut microbial diversity. However, position within the social network predicted gut microbial composition. These results emphasize the role of the social environment in determining the microbiota of adult animals. Since social transmission of gut microbiota has the potential to enhance immunity, microbiota might have played an escalating role in the evolution of sociality.

Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals

“…Other studies have focused on closely related mammal species and generally found that host species and their gut microbes exhibit concordant relationships [8,[15][16][17][18], with the gut microbial communities of different host species forming distinct clusters [18][19][20]. Within single host species, some studies of humans and other primates have suggested that social contact patterns are the primary predictor of gut microbiome composition [21][22][23][24][25], whereas others have found that host genetics exerts a strong influence [26,27].…”

“…All non-flying mammals of Madagascar belong to either one of four endemic orderslemurs, tenrecs, carnivorans, or rodents-or are recent human introductions-African bush pigs [37], cattle, cats, or dogs [38]. Recent studies have shown that the gut microbiomes of wild lemurs reflect social group membership and seasonal changes in diet [24,25,39,40], but none yet have considered the microbiomes of co-occurring mammalian species.…”

Terrestriality and bacterial transfer: A comparative study of gut microbiomes in sympatric Malagasy mammals

“…Other studies have focused on closely related mammal species, and generally found that host species and their gut microbes exhibit concordant phylogenies (8,15–18), with the gut microbiomes of different host species forming distinct clusters (18–20). Within single host species, some studies of humans and other primates have suggested that social contact patterns are the primary predictor of gut microbiome composition (21–25), whereas others have found that host genetics exert a strong influence (26,27).…”

“…All non-flying mammals fall into either one of four endemic orders—lemurs, tenrecs, carnivorans, or rodents—or are recent human introductions—African bush pigs (38), cattle, cats, or dogs (39). Recent studies have shown that social contacts and diet influence the gut microbiomes of wild lemurs (24,25,40), but none have yet considered the microbiomes of co-occurring mammalian species.…”

Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes

“…Grieneisen et al, 2017) and lemurs (Eulemur rubriventer:Raulo et al, 2017). Gut microbiomes are 70 also more similar among socially connected than disconnected siblings and married couples (Dill-71McFarland et al, 2019).…”