A positive association between gut microbiota diversity and vertebrate host performance in a field experiment

Abstract

AbstractThe vertebrate gut microbiota is a critical determinant of organismal function, yet it remains unclear if and how gut microbial communities affect host fitness under natural conditions. Here, we investigate associations between growth rate (a fitness proxy) and gut microbiota diversity and composition in a field experiment with threespine stickleback fish (Gasterosteus aculeatus). We detected on average 63% more bacterial taxa in the guts of high-fitness fish compared to low-fitness fish (i.e., higher α-diversity), suggesting that higher diversity promotes host growth. The microbial communities of high-fitness fish had higher similarity (i.e., lower β-diversity) than low-fitness fish, supporting the Anna Karenina principle— that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our findings provide a basis for functional tests of the fitness consequences of host-microbiota interactions.Significance statementThe vertebrate gut microbiota is important for many aspects of their hosts’ biology—such as nutrient metabolism and defense against pathogens—that could ultimately affect host fitness. However, studies investigating the effects of gut microbiota composition on vertebrate host fitness under natural conditions remain exceedingly rare. We tested for associations between gut microbiota diversity and growth rate (a fitness proxy) in threespine stickleback fish reared in large outdoor ponds. We found evidence that a more diverse gut microbiota was predictive of higher growth rate and therefore increased host fitness. Notably, high-fitness fish had higher gut microbiota similarity to one another than did low-fitness fish, providing experimental evidence for the Anna Karenina principle—that there are fewer ways to have a functional microbiota than a dysfunctional microbiota—as it relates to host fitness.