Gut microbial compositions mirror caste‐specific diets in a major lineage of social insects

Abstract

SummarySocial insects owe their ecological success to the division of labour between castes, but associations between microbial community compositions and castes with different tasks and diets have not been extensively explored. Fungus‐growing termites associate with fungi to degrade plant material, complemented by diverse gut microbial communities. Here, we explore whether division of labour and accompanying dietary differences between fungus‐growing termite castes are linked to gut bacterial community structure. Using amplicon sequencing, we characterize community compositions in sterile (worker and soldier) and reproductive (queen and king) termites and combine this with gut enzyme activities and microscopy to hypothesise sterile caste‐specific microbiota roles. Gut bacterial communities are structured primarily according to termite caste and genus and, in contrast to the observed rich and diverse sterile caste microbiotas, royal pair guts are dominated by few bacterial taxa, potentially reflecting their specialized uniform diet and unique lifestyle.

Synergies Between Division of Labor and Gut Microbiomes of Social Insects

“…Similarly, we predict that the structure and function of worker and reproductive gut microbiomes diverge during colony growth (Figure 2). The gut microbiomes of termite reproductives indicate a transition from diverse to simplified communities from founding to maturity (Shimada et al, 2013;Benjamino and Graf, 2016;Inagaki and Matsuura, 2016;Diouf et al, 2018;Otani et al, 2019) (Figure 2), which has been suggested to be a consequence of specialization on reproduction and dependence on workers (Chouvenc and Su, 2017). Similarly, the gut microbiome of honey bee queens exhibits slight changes with age (Tarpy et al, 2015;Anderson et al, 2018), suggesting that physiological and dietary changes related to reproductive specialization and duration may influence gradual shifts the reproductive microbiota.…”

“…In some social insect clades, the reproductive caste microbiome is distinct and drastically simplified compared to that of the worker caste. Foraging lower termite reproductives generally lack symbiotic protists that dominate the worker guts (Shimada et al, 2013;Inagaki and Matsuura, 2016), and the reproductive caste of Termitidae termites shows reduced diversity and disparate bacterial community composition (Otani et al, 2019) compared to the worker caste (Dietrich et al, 2014;Otani et al, 2014Otani et al, , 2016Otani et al, , 2019. Honey bee queens also host a simplified bacterial community that is significantly reduced compared to workers (Kapheim et al, 2015;Tarpy et al, 2015;Anderson et al, 2018).…”

“…Similarly, the fungus-farming subfamily of the Termitidae exhibits differences in gut bacterial composition related to foodprocessing by temporal subcastes (Hinze et al, 2002;Hongoh et al, 2006;Li et al, 2015Li et al, , 2016. Termites also present differences among physical subcastes, where soldier microbiomes can be distinct from other subcastes (Hongoh et al, 2006;Shimada et al, 2013;Inagaki and Matsuura, 2016;Otani et al, 2019, but see Berlanga et al, 2011), and in highly polymorphic termites, such as the genus Macrotermes, minor and major workers and soldiers display variable microbiomes (Hongoh et al, 2006;Schnorr et al, 2019).…”

Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission

“…These unicellular eukaryotes can reach population sizes of 10 5 per host individual, representing 60% of total hindgut weight (Bignell, 2011;Brune, 2011). Nonetheless, the literature on host-microbiome interaction in insects in general and termites in particular is based primarily on their bacterial and fungal symbionts (e.g., Aanen et al, 2002;Engel and Moran, 2013;Mikaelyan et al, 2015aMikaelyan et al, , 2017aGraf, 2016;Diouf et al, 2018;Otani et al, 2019). This is partly because the mutualistic partnership with flagellates appears unique among insects, but also because of methodological difficulties.…”

Defensive Symbioses in Social Insects Can Inform Human Health and Agriculture

“…However, the defined social structures of eusocial insects may be useful for understanding and manipulating microbial transmission later in life. Reproductive queens have limited contact with other adult workers, for instance, and understanding when and how they share microbes with other castes could illuminate the social elements of microbial transmission (Otani et al, 2019). Microbiomes of distinct nest structures provide an interesting comparison to the idea of built environments (Sharma and Gilbert, 2018).…”