Extensive inheritance of gut microbial communities in a superorganismal termite

Abstract

Mutualistic co-evolution can be mediated by vertical transmission of symbionts between host generations. Organisms exhibit adaptations that ensure optimal microbial inheritance, yet the extent to which this applies to social insects, such as termites that have co-evolved with gut microbes, is poorly resolved. Here, we document consistent vertical transmission across colony generations of fungus-farming termites. Inherited bacteria comprise 44% of the microbiome, over 80 genera, and strains that are specific to termite pedigrees. We show that the superorganism, consisting of reproductives and workers, analogous to gametes and soma of an organism, is adapted to vertically transmit a distinct microbial community with high fidelity. Microbial inheritance is achieved because colony-founding reproductives are endowed with a set of non-random, environmentally-sensitive, and termite-specific gut microbes derived from their colonies of origin. Reproductives biparentally transmit these symbionts to offspring colony workers, where priority effects dictate the composition of the forming colony microbiome. Superorganismal gametes, the reproductives, are thus adapted to secure transmission of entire communities of specific, co-evolved microbes that are critical to the colony microbiome later retained by workers. Extensive vertical transmission aligns with evolutionary patterns of termite-bacterial co-diversification. This colony-level inheritance extends models of transmission from individual organisms to superorganisms, both of which demonstrate adaptations to retain symbiotic fidelity and mixed-mode transmission conducive to mutualism.