Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens

Abstract

Carrion beetles, Nicrophorus vespilloides, are reared on decomposing vertebrate carrion where larvae are exposed to high-density populations of carcass-derived bacteria. We previously showed that larvae do not become colonized with these bacteria, but instead are colonized with the gut microbiome of their parents. These results suggested that bacteria in the beetle microbiome outcompete the carcass derived species for colonization of the larval gut. Here we test this hypothesis directly and quantify the fitness consequences of colonization of the Nicrophorus larval gut with different bacterial symbionts, including the insect pathogen Serratia marcescens. First, we show that beetles colonized by their endogenous microbiome produce significantly heavier broods than those colonized with carcass-bacteria. Next, we show that bacteria from the endogenous microbiome, including Providencia rettgeri and Morganella morganii, are better colonizers of the beetle gut and can outcompete non-endogenous species, including S. marcescens and Escherichia coli, during in vivo competition. Finally, we find that Providencia and Morganella provide beetles with colonization resistance against Serratia and thereby reduce Serratia-induced larval mortality during co-inoculation. Importantly, this effect is eliminated in larvae first colonized by Serratia, suggesting that while competition within the larval gut is strongly determined by priority effects, these effects are less important for Serratia-induced mortality. Our work supports the idea that bacterial gut symbionts provide direct benefits to Nicrophorus larvae by outcompeting potential bacterial pathogens. They further suggest that one benefit of parental care in Nicrophorus vespilloides is the social transmission of the microbiome from caring parents to their offspring.