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 .