Microbiome structure varied with geography and host
immunogenetics
Geography was a significant factor in microbiome structure (beta
diversity) for both bacterial and eukaryotic microbes. However,
microbiome structure was not associated with genetic structure of
populations at either neutral genetic markers or the MHC IIB
immunogenetic locus. These results differ from a previous study on the
frog Amietia hymenopus, which showed opposite patterns: there
were no geographic effects on amphibian skin microbiome structure, but
there was a significant association with population genetic structure
(29). One possible explanation for the discrepancy between our results
and the results from A. hymenopus (barring host identity factors)
is that geographic structure in the host-associated microbial community
is scale-dependent: our study spans a larger geographic area
(~100 km compared with ~4 km in
Griffiths et al. 2018). In addition, our study populations represent a
set of connected mainland populations contrasted with a set of island
populations that have been isolated for 12,000-20,000 years. The lack of
association with genetic differentiation in our populations may be due
to this relatively long period of divergence, or to isolation between
island sites resulting in different environmental availability of
microbes.
Microeukaryote diversity was associated with host genetic diversity,
with genetically impoverished island populations possessing lower
microeukaryotic diversity relative to coastal mainland populations (85.5
average OTUs on islands vs. 110.5 in coastal sites). This difference in
microbiome diversity could be due to a number of factors, including less
favorable environments or lower rates of host contact (i.e. ,
microbial transmission) on islands compared with coastal sites. However,
MHC IIB heterozygosity was positively associated with microeukaryotic
diversity even when only coastal populations were analyzed (19.2 average
OTUs on coastal homozygotes vs. 39.1 on coastal heterozygotes). Taken
together, these results imply that genetic diversity and/or MHC IIB
genotype plays a significant role in determining microbiome diversity.
Microbiome structure also varied across site types and MHC IIB
genotypes. Variation in microbiome structure among site types could be
parsimoniously explained by variation in environmental filtering in
coastal vs. island sites. However, these differences may also be driven
by island isolation favoring longer-dispersing microbes, or
alternatively by host genetic factors. The variation in microbiome
structure across MHC IIB genotypes, although weaker than the variation
due to site type, may be a clearer example of associations between
endogenous host factors and the microbiome. Although MHC genes are
thought to be primarily involved in pathogen resistance, results from
laboratory and field studies suggest that MHC genotype and allelic
composition can impact amphibian host-associated microbial assemblages
(30,63). Together with our finding that microbiome structure and
diversity are influenced by MHC genotype, this suggests that immune
mechanisms conferred by MHC genes may influence the assembly of the
overall microbiome.