Nonadaptive radiation of the gut microbiome in an adaptive radiation of Cyprinodon pupfishes with minor shifts for scale-eating

Abstract

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 trophic specialists, a scale-eater and a molluscivore, to a set of four outgroup generalist populations from which this adaptive radiation originated. We predicted an adaptive and highly divergent microbiome composition in the specialists matching their rapid rates of craniofacial diversification in the past 10 kya. We measured gut lengths and sequenced 16S rRNA amplicons of gut microbiomes from lab-reared fish fed the same high protein diet for one month. In contrast to our predictions, gut microbiota largely reflected 5 Mya phylogenetic divergence times among generalist populations in support of phylosymbiosis. However, we did find significant enrichment of Burkholderiaceae bacteria in both 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 Planctomycetacia in lab-reared molluscivore populations, but these bacteria target cellulose. Minor shifts in gut microbiota appear adaptive for scale-eating in this radiation, whereas overall microbiome composition was phylogenetically conserved. This 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 microbiome divergence proceeds as a nonadaptive radiation.

We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

“…Craniofacial morphology is one of the rapidly diversifying traits in this system, suggesting that divergence in daam2 may play a role in the shared craniofacial divergence of the two scale-eating species. Similarly, usp50 functions in protein metabolism and deubiquination [35] and may play a role in shared metabolic adaptations to the higher-protein content of a scale-eating or snail-eating diet (also note microbiome divergence of C. desquamator with increased prevalence of collagenase-digesting bacteria when reared in a common garden:[36]). atp8a1 is an ion transporter [37], znf214 is a transcription binding factor, and the ten unannotated variants were not associated with lower jaw size variation in a previous genome-wide association study of the radiation (Richards et al 2021).…”

“…Propionates and other short chain fatty acids are common microbiome metabolites [102]. A recent microbiome study in lab- reared populations found that C. desquamator microbiomes appear enriched for Burkholderiaceae bacteria that can digest collagen, further supporting an adaptive role for microbiomes in the radiation [73].…”

“…We found 6 shared hard selective sweeps in both species containing a total of 15 SNPS that were fixed or nearly-fixed compared to the sympatric generalist C. variegatus (figure 4E, 5): 10 SNPs were in unannotated regions, two were in the introns of the gene daam2, and three were in putative regulatory regions (with 20-kb) of the genes usp50, atp8a1, and znf214 (one variant each). Shared adaptive alleles in the gene daam2, a wnt signaling regulator, are intriguing because knockdown of this gene causes abnormal snout morphology in mice [35] and abnormal cranial and skeletal development in zebrafish [36].…”

“…desquamator with increased prevalence of collagenase-digesting bacteria when reared in a common garden: [36]). atp8a1 is an ion transporter [37], znf214 is a transcription binding factor, and the ten unannotated variants were not associated with lower jaw size variation in a previous genome-wide association study of the radiation (Richards et al 2021).…”