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.
Eco-evolutionary theory has brought an interest in the rapid evolution of functional traits. Among them, diet is an important determinant of ecosystem structure, affecting food web dynamics and nutrient cycling. However, it is largely unknown whether diet, or diet preference, has a hereditary basis and can evolve on contemporary timescales. Here, we study the diet preferences of Trinidadian guppies
Poecilia reticulata
collected from directly below an introduction site of fish transplanted from a high-predation environment into a low predation site where their densities and competition increased. Behavioural assays on F2 common garden descendants of the ancestral and derived populations showed that diet preference has rapidly evolved in the introduced population in only 12 years (approx. 36 generations). Specifically, we show that the preference for high-quality food generally found in high-predation guppies is lost in the newly derived low-predation population, who show an inertia toward the first encountered food. This result is predicted by theory stating that organisms should evolve less selective diets under higher competition. Demonstrating that diet preference can show rapid and adaptive evolution is important to our understanding of eco-evolutionary feedbacks and the role of evolution in ecosystem dynamics.
We took advantage of a five-decade ‘chronosequence’ of host-microbiome
evolution to examine changes in the gut microbiome as wild populations
evolve. In an iconic example of rapid evolution in the wild, Trinidadian
guppies have displayed parallel phenotypic convergence when translocated
six times from high predation (HP) to low predation (LP) environments,
but changes in microbiome are unknown. We find microbiomes of fish
translocated 5-6 years ago were already more similar to LP native
populations than HP sources, and attribute this to both environmental
and host-morphological changes. While diet was a minor driver of
microbiome structure, we suggest a nutritional role for the gut
microbiome in guppy evolution whereby nitrogen-fixing bacteria
supplement the low-nutrient diet in LP environments. We show that
environment and rapid phenotypic shifts in gut traits interact to
control microbiome assembly, and suggest the gut microbiome plays an
important but not necessarily consistent role in rapid host evolution.
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