Nonadaptive radiation of the gut microbiome in an adaptive radiation of
Cyprinodon pupfishes with minor shifts for scale-eating
- Joseph Heras,
- Christopher Martin
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.