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Adaptive radiations offer an excellent opportunity to understand the eco-evolutionary dynamics of gut microbiota and host niche specialization. In a laboratory common garden, we compared the gut microbiota of two novel derived trophic specialist pupfishes, a scale-eater and a molluscivore, to closely related and distant outgroup generalist populations, spanning both rapid trophic evolution within 10 kya and stable generalist diets persisting over 11 Mya. We predicted an adaptive and highly divergent microbiome composition in the trophic specialists reflecting their rapid rates of craniofacial and behavioral diversification. We sequenced 16S rRNA amplicons of gut microbiomes from lab-reared adult pupfishes raised under identical conditions and fed the same high protein diet. In contrast to our predictions, gut microbiota largely reflected phylogenetic distance among species, rather than generalist or specialist life history, in support of phylosymbiosis. However, we did find significant enrichment of Burkholderiaceae bacteria in replicated lab-reared scale-eater populations. These bacteria sometimes digest collagen, the major component of fish scales, supporting an adaptive shift. We also found some enrichment of Rhodobacteraceae and Planctomycetia in lab-reared molluscivore populations, but these bacteria target cellulose. Overall phylogenetic conservation of microbiome composition contrasts with predictions of adaptive radiation theory and observations of rapid diversification in all other trophic traits in these hosts, including craniofacial morphology, foraging behavior, aggression, and gene expression, suggesting that the functional role of these minor shifts in microbiota will be important for understanding the role of the microbiome in trophic diversification. 

Abstract Beyond a few obvious examples (e.g., gut length, amylase activity), digestive and metabolic specializations towards diet remain elusive in fishes. Thus, we compared gut length, δ¹³C and δ¹⁵N signatures of the liver, and expressed genes in the intestine and liver of wild-caught individuals of four closely-related, sympatric prickleback species (family Stichaeidae) with different diets:Xiphister mucosus(herbivore), its sister taxonX. atropurpureus(omnivore),Phytichthys chirus(omnivore) and the carnivorousAnoplarchus purpurescens. We also measured the same parameters after feeding them carnivore or omnivore diets in the laboratory for 4 weeks. Growth and isotopic signatures showed assimilation of the laboratory diets, and gut length was significantly longer inX. mucosusin comparison to the other fishes, whether in the wild, or in the lab consuming the different diets. Dozens of genes relating to digestion and metabolism were observed to be under selection in the various species, butP. chirusstood out with some genes in the liver showing strong positive selection, and these genes correlating with differing isotopic incorporation of the laboratory carnivore diet in this species. Although the intestine showed variation in the expression of hundreds of genes in response to the laboratory diets, the liver exhibited species-specific gene expression patterns that changed very little (generally <40 genes changing expression, withP. chirusproviding an exception). Overall, our results suggest that the intestine is plastic in function, but the liver may be where specialization manifests since this tissue shows species-specific gene expression patterns that match with natural diet.