Sexual reproduction brings genes from two parents (matrigenes and patrigenes) together into one individual. These genes, despite being unrelated, should show nearly perfect cooperation because each gains equally through the production of offspring. However, an individual's matrigenes and patrigenes can have different probabilities of being present in other relatives, so kin selection could act on them differently. Such intragenomic conflict could be implemented by partial or complete silencing (imprinting) of an allele by one of the parents. Evidence supporting this theory is seen in offspring-mother interactions, with patrigenes favoring acquisition of more of the mother's resources if some of the costs fall on half-siblings who do not share the patrigene. The kinship theory of intragenomic conflict is little tested in other contexts, but it predicts that matrigene-patrigene conflict may be rife in social insects. We tested the hypothesis that honey bee worker reproduction is promoted more by patrigenes than matrigenes by comparing across nine reciprocal crosses of two distinct genetic stocks. As predicted, hybrid workers show reproductive trait characteristics of their paternal stock, (indicating enhanced activity of the patrigenes on these traits), greater patrigenic than matrigenic expression, and significantly increased patrigenic-biased expression in reproductive workers. These results support both the general prediction that matrigene-patrigene conflict occurs in social insects and the specific prediction that honey bee worker reproduction is driven more by patrigenes. The success of these predictions suggests that intragenomic conflict may occur in many contexts where matrigenes and patrigenes have different relatednesses to affected kin. kinship theory | intragenomic conflict | evolutionary biology | social insects | sociogenomics
Populations of honey bees are declining throughout the world, with US beekeepers losing 30% of their colonies each winter. Though multiple factors are driving these colony losses, it is increasingly clear that viruses play a major role. However, information about the molecular mechanisms mediating antiviral immunity in honey bees is surprisingly limited. Here, we examined the transcriptional and epigenetic (DNA methylation) responses to viral infection in honey bee workers. One-day old worker honey bees were fed solutions containing Israeli Acute Paralysis Virus (IAPV), a virus which causes muscle paralysis and death and has previously been associated with colony loss. Uninfected control and infected, symptomatic bees were collected within 20–24 hours after infection. Worker fat bodies, the primary tissue involved in metabolism, detoxification and immune responses, were collected for analysis. We performed transcriptome- and bisulfite-sequencing of the worker fat bodies to identify genome-wide gene expression and DNA methylation patterns associated with viral infection. There were 753 differentially expressed genes (FDR<0.05) in infected versus control bees, including several genes involved in epigenetic and antiviral pathways. DNA methylation status of 156 genes (FDR<0.1) changed significantly as a result of the infection, including those involved in antiviral responses in humans. There was no significant overlap between the significantly differentially expressed and significantly differentially methylated genes, and indeed, the genomic characteristics of these sets of genes were quite distinct. Our results indicate that honey bees have two distinct molecular pathways, mediated by transcription and methylation, that modulate protein levels and/or function in response to viral infections.
A northern population of snapping turtles (Chelydra serpentina) centred around Lake Sasajewun in the Wildlife Research Area in Algonquin Park, Ontario, has been studied and individually marked since 1972. From 1972 to 1985, annual mortality and survivorship of adult females had been estimated at 1 and 96.6%, respectively, and only six dead turtles were found. Lake Sasajewun's population of C. serpentina was estimated in 1978–1979 and 1984–1985 at 38 and 47 adults, respectively. From 1976 to 1987, total number of nests found in the study area remained fairly constant and there were no significant changes in mean clutch size, mean clutch mass, or mean egg mass. On the main nest site, recruitment from 1976 to 1987 was 1.15 (1.8%) new females per year. From 1987 to 1989, we found 34 dead adult snapping turtles in the Wildlife Research Area. Observations of freshly dead animals indicated that most were killed by otters (Lutra canadensis) during the turtles' winter hibernation. A few uninjured turtles also died of septicemia in early spring shortly after emerging from hibernation. The estimated number of adults in Lake Sasajewun was 31 in 1988–1989, and the minimum number of adult residents known to be alive in the lake dropped from 47 in 1986 to 16 in 1989. In 1986 and 1987, annual adult female survivorship was estimated at 80 and 55%, respectively, and estimated numbers of nesting females declined from 82 in 1986 to 71 and 55 in 1987 and 1988, respectively. The actual number of nests found declined by 38 and 20% over the same periods. Although no significant differences occurred in mean egg mass or mean clutch size between 1987 and 1989 and earlier years, the mean clutch mass in 1988 was larger than in 1977 or 1978. This difference appeared to be due to a gradual increase in the mean age and body size of breeding females rather than to density-dependent changes. Recruitment into the adult breeding female population in 1987–1989 remained less than two individuals per year. Hatchling survival and number of juveniles were low throughout the study. Our observations support the view that populations of species with high, stochastic juvenile mortality and long adult life spans may be decimated quickly by increased mortality of adult animals, particularly if numbers of juveniles and immigrants are low. Recovery of such populations should be very slow because of a lack of effective density-dependent response in reproduction and recruitment.
Diapause is the key adaptation allowing insects to survive unfavourable conditions and inhabit an array of environments. Physiological changes during diapause are largely conserved across species and are hypothesized to be regulated by a conserved suite of genes (a 'toolkit'). Furthermore, it is hypothesized that in social insects, this toolkit was co-opted to mediate caste differentiation between long-lived, reproductive, diapause-capable queens and short-lived, sterile workers. Using Bombus terrestris queens, we examined the physiological and transcriptomic changes associated with diapause and CO2 treatment, which causes queens to bypass diapause. We performed comparative analyses with genes previously identified to be associated with diapause in the Dipteran Sarcophaga crassipalpis and with caste differentiation in bumble bees. As in Diptera, diapause in bumble bees is associated with physiological and transcriptional changes related to nutrient storage, stress resistance and core metabolic pathways. There is a significant overlap, both at the level of transcript and gene ontology, between the genetic mechanisms mediating diapause in B. terrestris and S. crassipalpis, reaffirming the existence of a conserved insect diapause genetic toolkit. However, a substantial proportion (10%) of the differentially regulated transcripts in diapausing queens have no clear orthologs in other species, and key players regulating diapause in Diptera (juvenile hormone and vitellogenin) appear to have distinct functions in bumble bees. We also found a substantial overlap between genes related to caste determination and diapause in bumble bees. Thus, our studies demonstrate an intriguing interplay between pathways underpinning adaptation to environmental extremes and the evolution of sociality in insects.
BackgroundOrganisms typically face infection by diverse pathogens, and hosts are thought to have developed specific responses to each type of pathogen they encounter. The advent of transcriptomics now makes it possible to test this hypothesis and compare host gene expression responses to multiple pathogens at a genome-wide scale. Here, we performed a meta-analysis of multiple published and new transcriptomes using a newly developed bioinformatics approach that filters genes based on their expression profile across datasets. Thereby, we identified common and unique molecular responses of a model host species, the honey bee (Apis mellifera), to its major pathogens and parasites: the Microsporidia Nosema apis and Nosema ceranae, RNA viruses, and the ectoparasitic mite Varroa destructor, which transmits viruses.ResultsWe identified a common suite of genes and conserved molecular pathways that respond to all investigated pathogens, a result that suggests a commonality in response mechanisms to diverse pathogens. We found that genes differentially expressed after infection exhibit a higher evolutionary rate than non-differentially expressed genes. Using our new bioinformatics approach, we unveiled additional pathogen-specific responses of honey bees; we found that apoptosis appeared to be an important response following microsporidian infection, while genes from the immune signalling pathways, Toll and Imd, were differentially expressed after Varroa/virus infection. Finally, we applied our bioinformatics approach and generated a gene co-expression network to identify highly connected (hub) genes that may represent important mediators and regulators of anti-pathogen responses.ConclusionsOur meta-analysis generated a comprehensive overview of the host metabolic and other biological processes that mediate interactions between insects and their pathogens. We identified key host genes and pathways that respond to phylogenetically diverse pathogens, representing an important source for future functional studies as well as offering new routes to identify or generate pathogen resilient honey bee stocks. The statistical and bioinformatics approaches that were developed for this study are broadly applicable to synthesize information across transcriptomic datasets. These approaches will likely have utility in addressing a variety of biological questions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3597-6) contains supplementary material, which is available to authorized users.
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