Stream characteristics and gut morphology drive microbiome
composition
Abiotic stream characteristics were strong drivers of gut microbiome.
Since temperature and pH are known drivers of microbial community
composition in freshwater (Fierer et al. 2007), such a
correlation might suggest that these factors are influencing gut
microbiome by exerting selection on the species pool (stream microbiota)
that colonizes the gut. However, this is not supported by Sullamet al. (2015), who found little overlap between guppy gut
microbiomes and their respective stream water. Alternatively, abiotic
variables could shape gut microbiome through other processes than
selection on the stream species, such as influencing prey, and their
associated microbial colonists (Jacobsen et al. 1997; Smithet al. 2015). While the mechanism of how exactly stream
properties affect microbiome is unresolved, it does suggest that
vertical transmission from parent to offspring does not overcome the
effect of site-specific factors on gut assembly, even in live-bearing
species.
An equally important driver of microbiome composition was gut length,
which, like the microbiome, shifted from the typical HP phenotype to
more closely resemble the LP phenotype, even in recent introductions.
Gut length is known to diverge in parallel between HP and LP ecotypes
(Zandonà et al. 2015) as more omnivorous LP guppies evolve longer
intestines to help with nutrient absorption in the lower-resource LP
environment. While adaptive evolution has been shown to occur rapidly in
this system (Reznick et al. 2019), the change in gut length may
also reflect phenotypic plasticity. Zandonà et al. (2015)
previously showed that differences between HP and LP guppy gut lengths
are smaller during the wet season when HP are more omnivorous. This
trait may be phenotypically plastic in other organisms, particularly
under fluctuating resource availability (Grether et al. 2001; Keet al. 2008), since digestive tissues are costly to maintain and
build (Sibly et al. 1981). Regardless of the mechanism by which
guts grew longer in LP environments, our study suggests that phenotypic
change in host traits drives microbiome change. Since both stream
properties and gut length had already shifted in the most recent
introductions (5-6 years in novel environment), we could not parse out
which was a stronger driver of gut composition. Future studies could ask
how the microbiome impacts host colonization of new site by capturing
generations immediately after translocation (or invasion), and also by
characterizing environmental microbiome, like those in water and on
prey.
Diet can alter gut microbiome in two ways: through changes in the
materials entering the gut, which affect microbiome colonization and
filtering, and through nutritional changes, which alter digestive traits
like gut morphology and chemistry. In our study, gut content played a
small role in driving microbiome composition, compared to shifts in gut
morphology. This is supported by previous work on guppies, which showed
that HP and LP fish retain different microbiomes even when fed the same
diet (Sullam et al. 2015), and at broad taxonomic scales, where
microbiome divergence track diet primarily in accordance with evolution
of in digestive traits (e.g. hindgut to foregut) (Muegge et al.2011). Gut content may primarily affect microbiome (particularly the
relative abundance of taxa) when gut morphology is held constant, or
when gut content matches aggregated diet. Gut content may not have
reflected typical HP and LP diets in our study due to time of sampling
(Zandonà et al. 2015, 2017). At the same time, if seasonal diet
shifts result in plastic morphological changes, this could be equally
powerful in altering gut microbiome. As our understanding of microbiome
divergence begins to extend beyond controlled studies, it will be
important to capture the complexity of diet in the wild, which may be
temporally dynamic (Colston & Jackson 2016), influenced by complex
behaviors, and not easily characterized by single axes induced in the
laboratory.