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.

The sustainable control of many highly damaging insect crop pests and disease vectors is threatened by the evolution of insecticide resistance. As a consequence, strategies have been developed that aim to prevent or delay resistance development by rotating or mixing insecticides with different modes of action (MoA). However, these approaches can be compromised by the emergence of mechanisms that confer cross-resistance to insecticides with different MoA. Despite the applied importance of cross-resistance, its evolutionary underpinnings remain poorly understood. Here we reveal how a single gene evolved the capacity to detoxify two structurally unrelated insecticides with different MoA. Using transgenic approaches we demonstrate that a specific variant of the cytochrome P450 CYP6ER1, previously shown to confer resistance to the neonicotinoid imidacloprid in the brown planthopper, N. lugens, also confers cross-resistance to the phenylpyrazole ethiprole. CYP6ER1 is duplicated in resistant strains, and we show that while the acquisition of mutations in two encoded substrate recognition sites (SRS) of one of the parologs led to resistance to imidacloprid, a different set of mutations, outside of known SRS, are primarily responsible for resistance to ethiprole. Epistatic interactions between these mutations and their genetic background suggest that the evolution of dual resistance from the same gene copy involved functional trade-offs in respect to CYP6ER1 catalytic activity for ethiprole versus imidacloprid. Surprisingly, the mutations leading to ethiprole and imidacloprid resistance do not confer the ability to detoxify the insecticide fipronil, another phenylpyrazole with close structural similarity to ethiprole. Taken together, these findings reveal how gene duplication and divergence can lead to the evolution of multiple novel functions from a single gene. From an applied perspective they also demonstrate how cross-resistance to structurally unrelated insecticides can evolve, and illustrate the difficulty in predicting cross-resistance profiles mediated by metabolic mechanisms.

Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations-for reasons that remain unclear.

There is an on-going need to develop new insecticides that are not compromised by resistance and that have improved environmental profiles. However, the cost of developing novel compounds has increased significantly over the last two decades. This is in part due to increased regulatory requirements, including the need to screen both pest and pollinator insect species to ensure that pre-existing resistance will not hamper the efficacy of a new insecticide via cross-resistance, or adversely affect non-target insect species. To add to this problem the collection and maintenance of toxicologically relevant pest and pollinator species and strains is costly and often difficult. Here we present Fly-Tox, a panel of publicly available transgenic Drosophila melanogaster lines each containing one or more pest or pollinator P450 genes that have been previously shown to metabolise insecticides. We describe the range of ways these tools can be used, including in predictive screens to avoid pre-existing cross-resistance, to identify potential resistance-breaking inhibitors, in the initial assessment of potential insecticide toxicity to bee pollinators, and identifying harmful pesticide-pesticide interactions.

A complex series of mutational events protected a mutualistic symbiosis during the shift of an insect to a toxic host plant.

Although cooperative social interactions within species are considered an important driver of evolutionary change, few studies have experimentally demonstrated that they cause adaptive evolution. Here we address this problem by studying the burying beetle Nicrophorus vespilloides. In this species, parents and larvae work together to obtain nourishment for larvae from the carrion breeding resource: parents feed larvae and larvae also self-feed. We established experimentally evolving populations in which we varied the assistance that parents provided for their offspring and investigated how offspring evolved in response. We show that in populations where parents predictably supplied more care, larval mandibles evolved to be smaller in relation to larval mass, and larvae were correspondingly less self-sufficient. Previous work has shown that antagonistic social interactions can generate escalating evolutionary arms races. Our study shows that cooperative interactions can yield the opposite evolutionary outcome: when one party invests more, the other evolves to invest less.

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.

. Some group-living species exhibit social immunity, where the immune response 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 approximately 1000 times to become one of the most abundant transcripts in the transcriptome. Females varied considerably in the antimicrobial properties of their anal exudates, and this was strongly correlated with the expression of this lysozyme. We conclude that we have likely identified a gene encoding a key effector molecule in social immunity and that it was recruited during evolution from a function in personal immunity.
.

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.

Division of labor is a complex phenomenon observed throughout nature. Theoretical studies have focused either on its emergence through self-organization mechanisms or on its adaptive consequences. We suggest that the interaction of self-organization, which undoubtedly characterizes division of labor in social insects, and evolution should be further explored. We review the factors empirically shown to influence task choice. In light of these factors, we review the most important self-organization and evolutionary models for division of labor and outline their advantages and limitations. We describe ways to unify evolution and self-organization in the theoretical study of division of labor and recent results in this area. Finally, we discuss some benchmarks and primary challenges of this approach.