Consistent divergence and drainage-specific convergence of gut microbiomes
We investigated variation in the guppy gut microbiome along an evolutionary ‘chronosequence’ of time-since-introduction, hypothesizing that gut microbiota tracks the evolution of fish traits such as gut morphology. Our hypothesis was supported in that, when HP fish were introduced into LP sites, their gut morphology changed to resemble that of LP native populations, and their microbiomes tracked this change. Coevolution of host and microbiome has been observed in macroevolutionary studies (Ley et al. 2008; Muegge et al.2011), but not always in replicate, independent divergences in the wild (Sevellec et al. 2018; Härer et al. 2020). We uniquely show that coevolution not only occurs but can be quite rapid; in our study, HP guppies translocated to LP environments after 5-6 years (approximately 15-18 guppy generations) were already more similar to native LP fish, despite their genetic background being more similar to their HP source populations (Fitzpatrick et al. 2015). This rapid microbiome divergence was driven by shifts in phenotypic traits and environment, suggesting that these factors are equally important for driving microbiome as diet and host genetics, which are more commonly studied.
While we observed dramatic and consistent divergence from HP microbiomes toward LP native microbiomes, even in the first 5 years after translocation, we did not observe consistent convergence of introduced populations with LP natives in every drainage. Although we cannot be sure, lack of convergence with LP natives does not appear to due to insufficient time. Some of the most recent introduced populations were indistinguishable from LP native microbiomes (Guanapo drainage), while one of the oldest introductions (El Cedro, 57 years in LP environment) remained distinct from LP natives. Abiotic differences among sites most strongly explained why LP and introduced microbiomes were not more similar. But while these site-specific effects led Sullamet al. (2015) to rule out parallel microbiome co-evolution in this system (because LP populations did not converge) our larger study suggests this should not be ruled out. Rather, the consistent divergence from HP source, drainage-dependent convergence with LP natives, and potential mechanisms for microbiomes to impact nutrition (see third section) suggest the gut microbiome affects host evolution while in the context of other agents influencing microbiome assembly (e.g. horizontal transmission). We further point out that parallelism at the functional level could occur without documenting consistent parallelism at the taxonomic level, especially given high functional redundancy in microbial communities (Louca et al. 2017).