Introduction
The gastrointestinal (GI) microbiome plays a critical role in host
fitness by facilitating nutrient absorption and producing metabolites
that influence interaction with the ecological niche , tissue
homeostasis , the immune system , and behavior . The host-microbe
relationship begins during development and changes throughout life
depending on environmental variables like diet . Host-driven mechanisms
that shape microbiome composition may provide individuals with a
selective advantage . Variation in the microbiome is always less within
a species than between species and as host species diverge, microbial
communities become more distinct . This phenomenon, also known as
phylosymbiosis, has been demonstrated in deer mice, mosquitos, and great
apes . However, the host genetic changes that underlie the evolution of
microbiome composition are largely unknown and challenging to
investigate in most systems. Such studies require comparing the
microbiomes of closely related genetically tractable species or
populations that have adapted to known environments. Studying divergent
populations of the same species thrust into similar conditions would
allow investigation of parallel development of host genetic mechanisms
that select for microbial communities.
In this study, we use river and cave adapted populations of the Mexican
tetra, Astyanax mexicanus , to investigate how adaptation to new
habitats shapes host-driven intestinal microbiome composition. A.
mexicanus is a single species of fish consisting of river-adapted
surface fish and multiple eyeless cave-adapted cavefish populations
named for the dark limestone caves they inhabit in Northeastern Mexico
(e.g., Tinaja, Molino, Pachón, Figure 1A-G ). Cavefish have
adapted to an environment with no light, reduced temperature variability
, low oxygen , limited nutrients , reduced competition , and altered
parasite diversity . Cavefish populations exhibit similar changes in
their morphology, like eye loss and reduced pigmentation , physiology,
like starvation resistance and hyperphagia , and behavior, like loss of
schooling and reduced sleep . Based on whole genome sequencing theA. mexicanus phylogeny defines two lineages; Tinaja and Pachón
cavefish form a monophyletic clade separate from Molino cavefish and Río
Choy surface fish . This evolutionary history indicates that cavefish
traits may have evolved through repeated evolution.
Researchers have bred surface fish and cavefish in laboratories for
generations to study the genetic and developmental basis of cavefish
traits like reduced aggression , increased fat accumulation , and
insulin resistance . These traits have been linked with microbiome
composition in other species . Characterizing the microbiome of A.
mexicanus therefore represents an important step in understanding
cavefish evolution. A previous study that compared the stomach
microbiome of two field collected Pachón cavefish and four field
collected surface fish suggested that dissolved oxygen, more so than
morphotype identity, determined microbial community composition . Here
we characterize the intestinal microbiome of cavefish and surface fish
that were collected in the field or raised in the laboratory to ask: (1)
Do cavefish and surface fish in their natural habitat have different
microbiomes? (2) How similar are the microbiomes of wild and laboratory
raised A. mexicanus ? (3) Does host evolutionary history shape
microbiome composition in A. mexicanus ? As anticipated, we found
that the microbiome is impacted by habitat. Our data shows that
laboratory raised fish harbor a more diverse microbiome that is
significantly different in composition compared to their wild
counterparts. More surprisingly, we found that host genetics alone can
explain differences in microbiome composition between surface fish and
cavefish. In addition, we found stable differences in abundance of taxa
with potential functional significance that can be used for quantitative
trait loci mapping to identify the genetic basis of host-mediated
microbiome composition. Our study defines the variables that shape the
microbiome in a model system that will continue to impact our
understanding of ecology and evolution due to its unique phylogeny ,
amenability to laboratory manipulation , and genetic accessibility .