Larval environmental conditions influence plasticity in resource use by adults in the burying beetle, Nicrophorus vespilloides.
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ABSTRACT:
SUBMITTER: Schrader M
PROVIDER: S-EPMC9293066 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description: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.
| S-EPMC4795035 | biostudies-literature
Project description:Nicrophorus vespilloides is a social beetle that rears its offspring on decomposing carrion. Wild beetles are frequently associated with two types of macrobial symbionts, mites, and nematodes. Although these organisms are believed to be phoretic commensals that harmlessly use beetles as a means of transfer between carcasses, the role of these symbionts on N. vespilloides fitness is poorly understood. Here, we show that nematodes have significant negative effects on beetle fitness across a range of worm densities and also quantify the density-dependent transmission of worms between mating individuals and from parents to offspring. Using field-caught beetles, we provide the first report of a new nematode symbiont in N. vespilloides, most closely related to Rhabditoides regina, and show that worm densities are highly variable across individuals isolated from nature but do not differ between males and females. Next, by inoculating mating females with increasing densities of nematodes, we show that worm infections significantly reduce brood size, larval survival, and larval mass, and also eliminate the trade-off between brood size and larval mass. Finally, we show that nematodes are efficiently transmitted between mating individuals and from mothers to larvae, directly and indirectly via the carcass, and that worms persist through pupation. These results show that the phoretic nematode R. regina can be highly parasitic to burying beetles but can nevertheless persist because of efficient mechanisms of intersexual and intergenerational transmission. Phoretic species are exceptionally common and may cause significant harm to their hosts, even though they rely on these larger species for transmission to new resources. However, this harm may be inevitable and unavoidable if transmission of phoretic symbionts requires nematode proliferation. It will be important to determine the generality of our results for other phoretic associates of animals. It will equally be important to assess the fitness effects of phoretic species under changing resource conditions and in the field where diverse interspecific interactions may exacerbate or reduce the negative effects of phoresy.
| S-EPMC6342123 | biostudies-literature
Project description:Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch 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 with bacteria from the carcass. More importantly, larvae receiving only prehatch 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 an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus 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 apparently 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 suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.
| S-EPMC5394326 | biostudies-literature
Project description:The increasing prevalence of antibiotic-resistant human pathogens is a growing public concern and there is intense pressure to identify new antibacterial compounds that can be developed into antibiotics with novel mode of action. Evolutionary theory predicts that insects that have evolved to occupy sophisticated ecological niches by feeding and reproducing on carcasses will depend on their gut microbiome to prevent colonization by invading pathogens taken up with the diet. This inspired our hypothesis that the complex interactions between the core microbiome and the more flexible microbial communities dependent on the environment may promote the outsourcing of antibiotic synthesis to beneficial microbes. We tested this hypothesis by cultivating and characterizing bacteria isolated from the gut of the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses buried in the soil to avoid competitors such as fly maggots. The extracts of isolated bacteria were screened for activity against human pathogens such as Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, and Candida albicans. More than 400 strains were isolated, among which the crude extract of Serratia marcescens 2MH3-2 displayed promising activity against Staphylococcus aureus. Bioactivity-guided fractionation enabled purification of the primary antimicrobial compound of the extract. By LC-MS and NMR experiments, it was identified as serrawettin W2 (C38H61N5O9), the antibacterial and nematostatic activity of which was corroborated in our study. We postulate that this antibiotic could contribute to the control of both bacteria and phoretic nematodes in the gut, which compete for food when transferred to the carcass. Our study shows that the gut microbiome of N. vespilloides is a promising resource for the screening of antibiotic-producing bacteria.
| S-EPMC6563848 | biostudies-literature
Project description:Sensory cues predicting resource quality are drivers of key animal behaviors such as preference or aversion. Despite the abundance of behavioral choice studies across the animal kingdom, relatively few studies have tested whether these decisions are driven by preference for one choice or aversion to another. In the burying beetle Nicrophorus vespilloides, adult pairs exhibit parental care to raise their offspring on a small carrion resource. We tested whether carrion decomposition stage affected brood quantity and quality and found that mating pairs had significantly more offspring on fresher carcasses. To determine whether this observed reproductive benefit correlates with maternal preference behavior, we conducted a series of olfactory trials testing mated female preferences for mouse carcasses of differing decomposition stages. When given the option between fresh and older carcasses, females associated significantly more with fresher, 1-day old carcasses. However, this behavior may be driven by aversion, as females that were given a choice between the 7-day old carcass and a blank control spent significantly more time in the control chamber. We characterized volatile organic compound profiles of both carcass types, highlighting unique compounds that may serve as public information (sensu lato) conveying resource quality information to gravid beetles.
| S-EPMC7824017 | biostudies-literature
Project description:Flexible behaviour allows organisms to respond appropriately to changing environmental and social conditions. In the subsocial beetle Nicrophorus vespilloides, females tolerate conspecifics when mating, become aggressive when defending resources, and return to social tolerance when transitioning to parenting. Given the association between octopamine and aggression in insects, we hypothesized that genes in the octopaminergic system would be differentially expressed across different social and reproductive contexts. To test this in N. vespilloides, we first obtained the sequences of orthologues of the synthetic enzymes and receptors of the octopaminergic system. We next compared relative gene expression from virgin females, mated females, mated females alone on a resource required for reproduction and mated females on a resource with a male. Expression varied for five receptor genes. The expression of octopamine β receptor 1 and octopamine β receptor 2 was relatively higher in mated females than in other social conditions. Octopamine β receptor 3 was influenced by the presence or absence of a resource and less by social environment. Octopamine α receptor and octopamine/tyramine receptor 1 gene expression was relatively lower in the mated females with a resource and a male. We suggest that in N. vespilloides the octopaminergic system is associated with the expression of resource defence, alternative mating tactics, social tolerance and indirect parental care.
| S-EPMC4237177 | biostudies-literature
Project description:Phenotypic plasticity is important in the evolution of traits and facilitates adaptation to rapid environmental changes. However, variation in plasticity at the individual level, and the heritable basis underlying this plasticity is rarely quantified for behavioral traits. Alternative behavioral reproductive tactics are key components of mating systems but are not often considered within a phenotypic plasticity framework (i.e., as reaction norms). Here, using lines artificially selected for repeated mating rate, we test for genetic (G × E) sources of variation in reproductive behavior of male Nicrophorus vespilloides burying beetles (including signaling behavior), as well as the role of individual body size, in responsiveness to changes in social environment. The results show that body size influences the response of individuals' signaling behavior to changes in the social environment. Moreover, there was G × E underlying the responses of males to variation in the quality of social environment experienced (relative size of focal male compared to his rival). This shows that individual variation in plasticity and social sensitivity of signaling behavior can evolve in response to selection on investment in mating behavior, with males selected for high mating investment having greater social sensitivity.
| S-EPMC5024017 | biostudies-literature
Project description:Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates. We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male-male competition. Male and female genital shape responded rapidly to selection on repeated mating rate. High and low mating rate lines diverged from control lines after only 10 generations of selection. We also detected significant patterns of male and female genital shape coevolution among selection regimes. We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology. The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.
| S-EPMC5089618 | biostudies-literature
Project description:BackgroundMutualistic interactions with microbes can help insects adapt to extreme environments and unusual diets. An intriguing example is the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses. Its fungal microbiome is dominated by yeasts that potentially facilitate carcass utilization by producing digestive enzymes, eliminating cadaver-associated toxic volatiles (that would otherwise attract competitors), and releasing antimicrobials to sanitize the microenvironment. Some of these yeasts are closely related to the biotechnologically important species Yarrowia lipolytica.ResultsTo investigate the roles of these Yarrowia-like yeast (YLY) strains in more detail, we selected five strains from two different phylogenetic clades for third-generation sequencing and genome analysis. The first clade, represented by strain B02, has a 20-Mb genome containing ~ 6400 predicted protein-coding genes. The second clade, represented by strain C11, has a 25-Mb genome containing ~ 6300 predicted protein-coding genes, and extensive intraspecific variability within the ITS-D1/D2 rDNA region commonly used for species assignments. Phenotypic microarray analysis revealed that both YLY strains were able to utilize a diverse range of carbon and nitrogen sources (including microbial metabolites associated with putrefaction), and can grow in environments with extreme pH and salt concentrations.ConclusionsThe genomic characterization of five yeast strains isolated from N. vespilloides resulted in the identification of strains potentially representing new YLY species. Given their abundance in the beetle hindgut, and dominant growth on beetle-prepared carcasses, the analysis of these strains has revealed the genetic basis of a potential symbiotic relationship between yeasts and burying beetles that facilitates carcass digestion and preservation.
| S-EPMC8091737 | biostudies-literature
Project description: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.
| S-EPMC2706201 | biostudies-other