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

Abstract

Carrion beetles, Nicrophorus vespilloides, are reared on decomposing carrion where larvae are exposed to high populations of carcass‐derived bacteria. Larvae do not become colonized with these bacteria but instead are colonized with the gut microbiome of their parents, suggesting that bacteria in the beetle microbiome outcompete the carcass‐derived species for larval colonization. Here, we test this hypothesis and quantify the fitness consequences of colonization with different bacterial symbionts. First, we show that beetles colonized by their endogenous microbiome produce 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 nonendogenous species, including Serratia 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. This effect is eliminated in larvae first colonized by Serratia, suggesting that while competition within the larval gut is determined by priority effects, these effects are less important for Serratia‐induced mortality. Our work suggests that an unappreciated benefit of parental care in N. vespilloides is the social transmission of the microbiome from parents to offspring.

Changes of gene expression but not cytosine methylation are associated with male parental care reflecting behavioural state, social context, and individual flexibility

“…Before offspring are born there is indirect care involving stripping the fur (or feathers or scales) from the carcass, forming it into a nest, and preventing microbial growth on the carcass through excretions (e.g. Palmer et al, 2016;Duarte et al, 2018;Shukla et al, 2018;Wang and Rozen, 2018). The latter form of indirect care also occurs after offspring are present, along with resource defence (Walling et al, 2008).…”

Heat production in a feeding matrix formed on carrion by communally breeding beetles

“…excretions) (52). They have antimicrobial effects (37) and, similarly to other carrion beetles (24, 26, 36, 42, 43), probably contain mutualistic microbes. Exudates may however also contain abiotic vectors of heat-generating processes, e.g.…”

“…Duarte et al (35) indicated that Nicrophorus beetles may seed carrion with their inner microbes or replant microbes from carcass gut to cadaver surface. Recent analyses of carrion beetle microbiomes recurrently reported the abundant presence of Yarrowia yeasts in beetle guts and in carrion biofilm, suggesting that there is a mutualistic link between the yeasts and carrion beetles (24, 26, 36, 42, 43). Microbial mutualists are probably associated also with Necrodes beetles, and the heat in a biofilm may support their growth or activity.…”

“…Moreover, some supposedly mutualistic microbes (e.g. Yarrowia yeasts) were abundantly identified in carrion beetle guts and carrion biofilm (24, 26, 36, 42, 43). Therefore, the biofilm-like matrix on carrion may be viewed as a result of carrion manipulation by beetles.…”

Fitness effects and transmission of phoretic nematodes of the burying beetle,Nicrophorus vespilloides

“…Nematodes can potentially cause indirect harm to beetle larvae by competing with them for space or resources, or possibly, by physically interfering with larvae while they consume the carcass. Phoretic nematodes are bacterivores, so direct resource competition with beetle larvae seems unlikely, unless some part of beetle nutrition is also microbial (directly or indirectly) (42). Competition for physical space may occur if nematode densities are sufficiently high to prevent larval feeding or access to parts of the carcass.…”