Insects that use ephemeral resources must rapidly digest nutrients and simultaneously protect them from competitors. Here we use burying beetles (Nicrophorus vespilloides), which feed their offspring on vertebrate carrion, to investigate the digestive and defensive basis of carrion utilization. We characterize gene expression and microbiota composition in the gut, anal secretions, and on carcasses used by the beetles. We find a strict functional compartmentalization of the gut involving differential expression of immune effectors (antimicrobial peptides and lysozymes), as well as digestive and detoxifying enzymes. A distinct microbial community composed of Firmicutes, Proteobacteria and a clade of ascomycetous yeasts (genus Yarrowia) is present in larval and adult guts, and is transmitted to the carcass via anal secretions, where the yeasts express extracellular digestive enzymes and produce antimicrobial compounds. Our results provide evidence of potential metabolic cooperation between the host and its microbiota for digestion, detoxification and defence that extends from the beetle's gut to its nutritional resource.
Despite a vast literature on the factors controlling adult size, few studies have investigated how maternal size affects offspring size independent of direct genetic effects, thereby separating prenatal from postnatal influences. I used a novel experimental design that combined a cross-fostering approach with phenotypic manipulation of maternal body size that allowed me to disentangle prenatal and postnatal maternal effects. Using the burying beetle Nicrophorus vespilloides as model organism, I found that a mother's body size affected egg size as well as the quality of postnatal maternal care, with larger mothers producing larger eggs and raising larger offspring than smaller females. However, with respect to the relative importance of prenatal and postnatal maternal effects on offspring growth, only the postnatal effects were important in determining offspring body size. Thus, prenatal effects can be offset by the quality of postnatal maternal care. This finding has implications for the coevolution of prenatal and postnatal maternal effects as they arise as a consequence of maternal body size. In general, my study provides evidence that there can be transgenerational phenotypic plasticity, with maternal size determining offspring size leading to a resemblance between mothers and their offspring above and beyond any direct genetic effects.
Carrion beetles (Coleoptera, Silphidae) are well known for their behaviour of exploiting vertebrate carcasses for nutrition. While species in the subfamily Silphinae feed on large carcasses and on larvae of competing scavengers, the Nicrophorinae are unique in monopolizing, burying and defending small carrion, and providing extensive biparental care. As a first step towards investigating whether microbial symbionts may aid in carcass utilization or defence, we characterized the microbial hindgut communities of six Nicrophorinae (Nicrophorus spp.) and two Silphinae species (Oiceoptoma noveboracense and Necrophila americana) by deep ribosomal RNA amplicon sequencing. Across all species, bacteria in the family Xanthomonadaceae, related to Ignatzschineriao larvae, were consistently common, and several other taxa were present in lower abundance (Enterobacteriales, Burkholderiales, Bacilli, Clostridiales and Bacteroidales). Additionally, the Nicrophorinae showed high numbers of unusual Clostridiales, while the Silphinae were characterized by Flavobacteriales and Rhizobiales (Bartonella sp.). In addition to the complex community of bacterial symbionts, each species of carrion beetle harboured a diversity of ascomycetous yeasts closely related to Yarrowia lipolytica. Despite the high degree of consistency in microbial communities across the Silphidae--specifically within the Nicrophorinae--both the fungal symbiont phylogeny and distance-based bacterial community clustering showed higher congruence with sampling locality than host phylogeny. Thus, despite the possibility for vertical transmission via anal secretions, the distinct hindgut microbiota of the Silphidae appears to be shaped by frequent horizontal exchange or environmental uptake of symbionts. The microbial community profiles, together with information on host ecology and the metabolic potential of related microorganisms, allow us to propose hypotheses on putative roles of the symbionts in carcass degradation, detoxification and defence.
Although chemical communication is the most widespread form of communication, its evolution and diversity are not well understood. By integrating studies of a wide range of terrestrial plants and animals, we show that many chemicals are emitted, which can unintentionally provide information (cues) and, therefore, act as direct precursors for the evolution of intentional communication (signals). Depending on the content, design and the original function of the cue, there are predictable ways that selection can enhance the communicative function of chemicals. We review recent progress on how efficacybased selection by receivers leads to distinct evolutionary trajectories of chemical communication.Because the original function of a cue may channel but also constrain the evolution of functional communication, we show that a broad perspective on multiple selective pressures acting upon chemicals provides important insights into the origin and dynamic evolution of chemical information transfer. Finally, we argue that integrating chemical ecology into communication theory may significantly enhance our understanding of the evolution, the design and the content of signals in general.
SignificanceEphemeral diets such as carrion are high-quality resources that are susceptible to microbial spoilage. Carrion-feeding insects that breed on decaying carcasses must overcome challenges arising from competing microbes. Here we report that a carrion-feeding burying beetle preserves carcasses by regulating its microbial growth, resulting in changes in its biochemical properties including the reduction of toxic polyamines associated with putrefaction and nutrient loss. The beetle’s microbial symbionts form a biofilm-like matrix on carcasses, which is important for optimal larval development. The beetles and their microbiome thus coordinate a specialized adaptive strategy of carrion management, enabling them to preserve carrion quality and support larval growth in a challenging resource such as carrion.
Studies on the evolution of parental care have focused primarily on the costs and benefits of parental care and the life-history attributes that favour it. However, once care evolves, offspring in some taxa appear to become increasingly dependent on their parents. Although offspring dependency is a central theme in family life, the evolutionary dynamics leading to it are not fully understood. Beetles of the genus Nicrophorus are well known for their elaborate biparental care, including provisioning of their young. By manipulating the occurrence of pre- or post-hatching care, we show that the offspring of three burying beetle species, N. orbicollis, N. pustulatus, and N. vespilloides, show striking variation in their reliance on parental care. Our results demonstrate that this variation within one genus arises through a differential dependency of larvae on parental feeding, but not on pre-hatching care. In N. pustulatus, larvae appear to be nutritionally independent of their parents, but in N. orbicollis, larvae do not survive in the absence of parental feeding. We consider evolutionary scenarios by which nutritional dependency may have evolved, highlighting the role of brood size regulation via infanticide in this genus.
The waxy layer of the cuticle has been shown to play a fundamental role in recognition systems of insects. The biparental burying beetle Nicrophorus vespilloides is known to have the ability to discriminate between breeding and non-breeding conspecifics and also here cuticular substances could function as recognition cue. However, it has not yet been demonstrated that the pattern of cuticular lipids can reflect the breeding status of a beetle or of any other insect. With chemical analysis using coupled gas chromatography-mass spectrometry, we showed that the chemical signature of N. vespilloides males and females is highly complex and changes its feature with breeding status. Parental beetles were characterized by a higher amount of some unusual unsaturated hydrocarbons than beetles which are not caring for larvae. The striking correlation between cuticular profiles and breeding status suggests that cuticular hydrocarbons inform the beetles about parental state and thus enable them to discriminate between their breeding partner and a conspecific intruder. Furthermore, we found evidence that nutritional conditions also influence the cuticular profile and discuss the possibility that the diet provides the precursors for the unsaturated hydrocarbons observed in parental beetles. Our study underlines the fact that the cuticular pattern is rich of information and plays a central role in the burying beetles' communication systems.
The burying beetle Nicrophorus vespilloides has emerged as a model system for the investigation of adaptations that allow the utilization of carrion as a diet and as a resource for reproduction. The survival of beetles and their offspring given their exposure to soil-dwelling and cadaver-borne microbes requires mechanisms that reduce bacterial contamination in the diet and that achieve sanitation of the microhabitat. To explore the role of antimicrobial peptides (AMPs) in this context, we analyzed burying beetle males and females at different stages of their breeding cycle using the RNA-Seq and proteomics approaches. To address variation in immune functions, we investigated the impact of adult sex, the presence or absence of offspring (social context), and the presence of carrion (environmental context) on the expression of the identified immune effector genes. We found that particular AMPs are sex-specific and tightly regulated by the presence of a carcass or offspring and identified the two most context-dependent antimicrobial proteins in anal secretions. The context-specific expression dynamics of particular AMPs and lysozymes reveals a complex regulatory system, reflecting adaptations to specific ecological niches. This study highlights how burying beetles cope with microorganisms found on carrion and identifies candidates for both internal and external immunity.
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