Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes

Abstract

Ecoevolutionary dynamics of the gut microbiota at the macroscale level, that is, in across-species comparisons, are largely driven by ecological variables and host genotype. The repeated explosive radiations of African cichlid fishes in distinct lakes, following a dietary diversification in a context of reduced genetic diversity, provide a natural setup to explore convergence, divergence and repeatability in patterns of microbiota dynamics as a function of the host diet, phylogeny and environment. Here we characterized by 16S rRNA amplicon sequencing the gut microbiota of 29 cichlid species from two distinct lakes/radiations (Tanganyika and Barombi Mbo) and across a broad dietary and phylogenetic range. Within each lake, a significant deviation between a carnivorous and herbivorous lifestyle was found. Herbivore species were characterized by an increased bacterial taxonomic and functional diversity and converged in key compositional and functional community aspects. Despite a significant lake effect on the microbiota structure, this process has occurred with remarkable parallels in the two lakes. A metabolic signature most likely explains this trend, as indicated by a significant enrichment in herbivores/omnivores of bacterial taxa and functions associated with fiber degradation and detoxification of plant chemical compounds. Overall, compositional and functional aspects of the gut microbiota individually and altogether validate and predict main cichlid dietary habits, suggesting a fundamental role of gut bacteria in cichlid niche expansion and adaptation.

Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

“…This gene is otherwise known to be used exclusively during the larval period in Nile tilapia (Spady et al, ). Similarly, we detected expression of the UV‐sensitive SWS1 opsin (expressed in larvae of Nile tilapia; Spady et al, ) in one species, S. steinbachi , an algae/debris feeder and the most herbivorous species from the lake (Baldo et al, ; Trewavas et al, ; and personal observation of higher plant feeding). The link between herbivory and SWS1 expression is in agreement with the observations of O'Quin et al () in Malawi cichlids, where algae scrapers (together with zooplanktivores) have increased expression levels of SWS1.…”

“…This gene is otherwise known to be used exclusively during the larval period in Nile tilapia (Spady et al, 2006). Similarly, we detected expression of the UV-sensitive SWS1 opsin (expressed in larvae of Nile tilapia; Spady et al, 2006) in one species, S. steinbachi, an algae/debris feeder and the most herbivorous species from the lake (Baldo et al, 2017;Trewavas et al, 1972; and personal ob-…”

“…Crater lake Barombi Mbo has a diameter of only 2.5 km but is more than 110 m deep (Trewavas, Green, & Corbet, ; Figure a) and hosts eleven endemic species of cichlid fishes ( Konia dikume , K. eisentrauti , Myaka myaka , Pungu maclareni , Sarotherodon steinbachi , S. lohbergeri , S. linnellii , S. caroli , Stomatepia mariae , St. mongo and St. pindu ; Figure c), which probably arose in situ following a colonization event no earlier than 1 million years ago (Cornen, Bande, Giresse, & Maley, ; Richards, Poelstra, & Martin, ; Schliewen & Klee, ). During this time frame, the species have diversified with respect to ecology, as documented by their trophic niche specialization (Baldo et al, ), as well as with respect to their water depth preference (Trewavas et al, ). While nine out of the eleven Barombi Mbo cichlid species are commonly and syntopically found in the shallow littoral zone of the crater lake, two species have colonized the deep‐water zone: (a) K. dikume is an obligatory deep‐water specialist that inhabits the zone at around 20 m of depth (Trewavas et al, ); and (b) M. myaka is a seasonal deep‐water species that occurs in the deep‐water habitat during the dry season (November–April), yet migrates into the shallow littoral zone for spawning during the peak of the rainy season (June–August) (Trewavas et al, ).…”

Amazon fish bacterial communities show structural convergence along widespread hydrochemical gradients

“…In the same manner, Sevellec et al () compared the intestinal microbiota of five sympatric pairs of dwarf (limnetic) and normal (benthic) lake whitefish ( Coregonus clupeaformis ) and did not detect a clear evidence for parallelism as similar microbiota taxonomic composition was only observed for two out of five, lake specific, sympatric species pairs. Contrastingly, in a study on African cichlid fishes, Baldo et al () did detect significant parallelism, as distinct herbivore species from different lakes converged both in terms of key compositional and functional community aspects associated with plant fibre degradation. Our results showed two levels of parallelism.…”

Evidence for host effect on the intestinal microbiota of whitefish (Coregonus sp.) species pairs and their hybrids

“…There is increasing evidence that allochthonous microbial communities (hereafter the transient microbiota) ingested from the environment by the host play a significant role in the overall gut microbiota, either by stimulating colonization resistance or by providing additional functions to the host (e.g., David et al, 2014). However, few studies have tested for parallelism patterns in fish intestinal microbiota (Baldo et al, 2017;Baldo, Riera, Tooming-Klunderud, Albà, & Salzburger, 2015;Hata et al, 2014;Sevellec et al, 2014;Smith, Snowberg, Caporaso, Knight, & Bolnick, 2015;Sullam et al, 2015). Also, the effect of the hybridization of two recently diverged species on microbiota composition is still poorly documented (Guivier et al, 2017).…”