Shifts in gut microbiome across five decades of repeated guppy translocations in Trinidadian streams

Abstract

An organism's 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.

Keywords: Poecilia reticulata; diet; gut microbiome; gut morphology; translocation.

Figure 1.

Map illustrating sampling scheme for our study on the island of Trinidad, and information for each site. Six translocation scenarios are indicated by dashed grey arrows with the names of rivers and year of translocation. Black squares represent high-predation source sites and yellow stars represent translocation sites. Native LP sites (green circles from west to east) are Tumbasson, Naranjo and Campo. Table shows site and sample descriptions, with the following footnotes: ^aGuts were further divided into anterior and posterior sections for microbiome characterization. ^bNote source of Turure introductions was Guanapo HP source, thus is sometimes compared to Guanapo sites, but is not located in Guanapo drainage. (Online version in colour.)

Figure 2.

Stream properties, fish traits and diet for each site, as organized by drainage (sections in each graph) and site category (colours), including mean (Site category). Error bars (some hidden) show standard error and are not shown for Site Category for clarity. *Represent p < 0.01 for equal means across site category. (Online version in colour.)

Figure 3.

Distance-based redundancy analysis based on the composition of bacterial guppy gut microbiomes (weighted Unifrac) in high and in LP streams, where HP fish (HP source, red) have been introduced either 30–60 years ago (Old Intro, green) or 5–6 years ago (Recent Intro, blue), and evolved to resemble native LP fish (black). (a) shows all site categories and (b) excludes HP source sites, showing sites in LP environments (LP native, old intro and recent intro). Arrows show the predictor variables that explain changes in composition based on dbRDA, and length corresponds to dbRDA R². Right barplots show the partial R² variance partitioned for diet, gut length and water temperature (grayscale). In the electronic supplementary material, you will find ordinations and barplots for all distance metrics (figures S4 and S5), drainage-specific ordinations (figure S6), dbRDA statistics (table S4) and PerMANOVA results (tables S2 and S3). (Online version in colour.)

Figure 4.

Dissimilarity (unweighted Unifrac distance) of the gut microbiome of each population compared to the gut microbiome of its HP source population (shown by a red line at 0). Higher values are more dissimilar to HP source. Inset of (a) shows finer scale axes. See electronic supplementary material, figure S7 for mean pairwise distances of all sites. Note that TR is sourced from the Guanapo HP site but because they are both in Oropouche drainage, serves as a comparison to Campo. (Online version in colour.)

Figure 5.

Gut microbiome richness (a), mean relative abundance of order Rhizobiales (b), relative abundance of five Rhizobiales species (categorized by genus, if known) that were part of the ten most abundant OTUs across all treatments (c), mean number of metabolic functions detected (d), nitrogenase copies (e) and chitinase copies (f). Bottom row panels are predicted from 16S copies using PICRUST2. Other community diversity metrics are shown in electronic supplementary material, figure S3, most abundant OTUs listed in electronic supplementary material, table S5, and site-level nitrogenase and chitinase are show in electronic supplementary material, figure S8. (Online version in colour.)