Some group-living species exhibit social immunity, where the immune system of one individual can protect others in the group from infection. In burying beetles this is part of parental care. Larvae feed on vertebrate carcasses which their parents smear with exudates that inhibit microbial growth. We have sequenced the transcriptome of the burying beetle Nicrophorus vespilloides and identified six genes that encode lysozymes – a type of antimicrobial enzyme that has previously been implicated in social immunity in burying beetles. When females start breeding and producing antimicrobial anal exudates, we found that the expression of one of these genes was increased by ~1000 times to become one of the most abundant transcripts in the transcriptome. We conclude that we have likely identified a gene for social immunity, and that it was recruited during evolution from a previous function in personal immunity.

AbstractIt is still poorly understood how animal behaviour shapes bacterial communities and their evolution. We use burying beetles, Nicrophorus vespilloides, to investigate how animal behaviour impacts the assembly of bacterial communities. Burying beetles use small vertebrate carcasses as breeding resources, which they roll into a ball, smear with antimicrobial exudates and bury. Using high-throughput sequencing we characterize bacterial communities on fresh mouse carcasses, aged carcasses prepared by beetles, and aged carcasses that were manually buried. The long-standing hypothesis that burying beetles ‘clean’ the carcass from bacteria is refuted, as we found higher loads of bacterial DNA in beetle-prepared carcasses. Beetle-prepared carcasses were similar to fresh carcasses in terms of species richness and diversity. Beetle-prepared carcasses distinguish themselves from manually buried carcasses by the reduction of groups such as Proteobacteria and increase of groups such as Flavobacteriales and Clostridiales. Network analysis suggests that, despite differences in membership, network topology is similar between fresh and beetle-prepared carcasses. We then examined the bacterial communities in guts and exudates of breeding and non-breeding beetles. Breeding was associated with higher diversity and species richness. Breeding beetles exhibited several bacterial groups in common with their breeding resource, but that association is likely to disappear after breeding.

Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.

Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass.

It is well-known that features of animal nest architecture can be explained by fitness benefits gained by the offspring housed within. Here we focus on the little-tested suggestion that the fitness costs associated with building and maintaining a nest should additionally account for aspects of its architecture. Burying beetles prepare an edible nest for their young from a small vertebrate carcass, by ripping off any fur or feathers and rolling the flesh into a rounded ball. We found evidence that only larger beetles are able to construct rounder carcass nests, and that rounder carcass nests are associated with lower maintenance costs. Offspring success, however, was not explained by nest roundness. Our experiment thus provides rare support for the suggestion that construction and maintenance costs are key to understanding animal architecture.