Evidence of cospeciation between termites and their gut bacteria on a geological time scale

Abstract

Termites host diverse communities of gut microbes, including many bacterial lineages only found in this habitat. The bacteria endemic to termite guts are transmitted via two routes: a vertical route from parent colonies to daughter colonies and a horizontal route between colonies sometimes belonging to different termite species. The relative importance of both transmission routes in shaping the gut microbiota of termites remains unknown. Using bacterial marker genes derived from the gut metagenomes of 197 termites and one Cryptocercus cockroach, we show that bacteria endemic to termite guts are mostly transferred vertically. We identified 18 lineages of gut bacteria showing cophylogenetic patterns with termites over tens of millions of years. Horizontal transfer rates estimated for 16 bacterial lineages were within the range of those estimated for 15 mitochondrial genes, suggesting that horizontal transfers are uncommon and vertical transfers are the dominant transmission route in these lineages. Some of these associations probably date back more than 150 million years and are an order of magnitude older than the cophylogenetic patterns between mammalian hosts and their gut bacteria. Our results suggest that termites have cospeciated with their gut bacteria since first appearing in the geological record.

Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite

“…By contrast, 13 genera that increased in abundance in founding reproductives completed vertical transmission across all pedigrees (figure 3 b ; electronic supplementary material, table S4) . These genera thus appear critical for hosts, consistent with findings that several have diversified with termite hosts [11,27] and are members of the core microbiome [34]. The subsequent transfer to offspring colonies did not drastically alter the inherited microbiome, but some inherited genera either significantly increased or decreased in relative abundance (electronic supplementary material, figure S4 and table S4).…”

“…These proximate patterns and association specificity may thus inform symbiotic evolution [6,7]. Indeed, our results align with termite-bacteria cladogenesis at evolutionary timescales, where lineages of bacterial symbionts exhibit distinct transmission modes, ranging from exclusive vertical transmission (strong co-cladogenesis) to predominant or exclusive horizontal transmission (lacking co-cladogenesis) [11,27]. Maturing colonies thus benefit from mixed-mode transmission that optimize tripartite associations between termite, fungus and bacterial microbiota at ecological timescales (microbial assembly) and over evolutionary time (extent of coevolution).…”

“…Thus, by comparing ASV transmission across four distinct pedigrees, we uncovered transmission at the genus and ASV level that involves extensive pedigree specificity and biparental contributions. This builds on recent work [11,27,31], but demonstrates inheritance of a core community with unprecedented resolution, consistency across genetic pedigrees and biparental contributions of bacteria that persist in offspring colonies. In accordance with our second hypothesis, we found that founding reproductives have the greatest impact on shaping the inherited microbiome and secure transmission of a non-random set of bacteria.…”

“…Termites are valuable models to examine the specificity and mechanisms of vertical transmission because of their 150 Myr long association with beneficial and complex gut microbiomes [23] that have co-adapted to serve digestive roles [24,25]. Co-cladogenesis of termite hosts with bacterial and protist symbionts indicates predominant vertical transmission punctuated by horizontal transmission from other hosts or the environment [11,[26][27][28]. Yet, the transmission between colony generations, which in part drives these evolutionary patterns, is not well understood.…”

The importance of host physical niches for the stability of gut microbiome composition

“…Applying a similar approach, numerous other groups have found similar co-phylogenetic diversification of host and microbe. Example hosts where this pattern occurs include sap sucking insects such as aphids [15], cicadas and sharpshooters [15,16], entomopathogenic nematodes and their bacterial symbionts [17], termites [18], stinkbugs [19][20][21], ants [22] and certain species of gut bacteria in primates [11,23]. While the sap sucking insects have intracellular bacteria that are vertically transmitted, the other associations are for gut bacteria, which are environmentally acquired.…”