An organisms’ gut microbiome can alter its fitness, yet we do not know how gut microbiomes change as their hosts evolve in the wild. We took advantage of a five-decade ‘chronosequence’ of translocated fish populations to examine associated changes in the gut microbiome. Populations of Trinidadian guppies have displayed parallel phenotypic convergence six times when moved from high predation (HP) to low predation (LP) environments. Across four drainages, we found microbiomes of fish translocated 5-6 years prior to sampling were already distinct from the microbiomes of their HP source populations. Changes in environmental conditions were most important in driving this shift, followed by phenotypic shifts in gut morphology. After 30-60 years in LP environments, microbiome composition was still distinct from native LP populations, but microbiome function was not. We found some evidence that nitrogen fixation enhanced gut nutrient absorption, but most functional shifts were not parallel across drainages. Stream-and drainage-specific signatures were present for both composition and function, despite our overall finding of consistent microbiome change across drainages. As we unravel the complexities of host-microbiome evolution in the wild, studies should consider environmental microbial colonization, host phenotypic plasticity in nature, and more realistic environmental conditions excluded from laboratory studies.

Researches collected guppy fish from Trinidadian streams and assessed stream characteristics (abiotic variables of water), fish morphological traits, contents of the gut to assess diet, and gut microbiome composition. For the latter, sequences are submitted to NCBI SRA (Bio-Project no. PRJNA259592) and bioinformatic code is publicly available (https://gitlab.msu.edu/belldere/guppy_gut_2015). Methods describing measurement of abiotic conditions, gut morphology, and gut content, are described in the manuscript (Methods and Supplementary methods). Details of the site locations and history are in Figure 1 in the MS.

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