Colonization and transmission of the gut microbiota of the burying beetle,Nicrophorus vespolloides, through development

Abstract

AbstractCarrion beetles in the genusNicrophorusrear their offspring on decomposing carcasses where larvae are exposed to a diverse microbiome of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as Pre-Hatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as Full care). Here we partition the roles of pre- and post-hatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (Full-Care, Pre-Hatch care only, and No Care), we found that larvae receiving Full-Care are predominantly colonized by bacteria resident in the maternal gut, while larvae receiving No Care are colonized exclusively with bacteria from the carcass. More importantly, larvae receiving only Pre-Hatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo a aposymbiotic stage, after which they are recolonized at eclosion with bacteria shed in the moulted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of pre-hatch parental care for symbiont transmission inNicrophorus vespilloides, and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.ImportanceHere we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetleNicrophorus vespilloides.This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses where they are exposed to high-densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation, but are recolonized from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further indicate that strong competitive interactions mediate the bacterial composition ofNicrophoruslarvae, suggesting that the bacterial communities of these insects may be highly coevolved with their host species.