Insights into social insects from the genome of the honey bee Apis mellifera

Nature (Impact Factor: 41.46). 10/2006;


ARTICLES Insights into social insects from the genome of the honeybee Apis mellifera The Honeybee Genome Sequencing Consortium* Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A1T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement. The western honeybee, Apis mellifera, is a striking creature, one of relatively few species for which evolution culminated in advanced society 1 . In 'eusocial' insect colonies, populations are differentiated into queens that produce offspring and non-reproductive altruistic workers that gather and process food, care for young, build nests and defend colonies. Remarkably, these two castes, both highly derived relative to solitary insects, develop from the same genome. Social evolution endowed honeybees with impressive traits 2,3 . Differentiation into queens and workers is through nutritionally based, hormone-mediated, programmes of gene expression 4 yielding dramatic distinctions in morphology, physiology and behaviour. Queens, typically one per colony, have ten times the lifespan of work-ers, typically 1 to 2 yr 5 , lay up to 2,000 eggs per day, and store sperm for years without losing viability. Workers, numbering tens of thou-sands per colony, display sophisticated cognitive abilities, despite a brain containing only one million neurons 6 . This is five orders of magnitude less than the human brain and only four times greater than Drosophila, which has a far simpler behavioural repertoire. Workers learn to associate a flower's colour, shape, scent, or location with a food reward 7 , increasing foraging efficiency. They commun-icate new food discoveries with 'dance language', originally deci-phered by von Frisch 8 , the only non-primate symbolic language. Recent studies revealed that honeybees can learn abstract concepts such as 'same' and 'different' 9 . The infamous African 'killer' bees, Apis mellifera scutellata, the queens of which were introduced to Brazil in 1956 10 , are known for intense stinging activity during nest defence, and pose human health problems. The African bees' spread throughout the New World is a spectacular example of biological invasion. Although it was one of the first biological invasions to be studied with molecular tools 11 , our understanding of its genetic basis has been controversial. This array of fascinating features, as well as amenability to molecu-lar, genetic, neural, ecological and social manipulation 12 , led to selec-tion of the honeybee for genome sequencing by the National Human Genome Research Institute, National Institutes of Health (NHGRI, NIH) 13 . The United States Department of Agriculture (USDA) also supported the project because of the paramount importance of pollination to human nutrition and the environment 14 . And, of course, humans and other animals have valued honey since prehis-toric times. Honeybees belong to the insect order Hymenoptera, which includes 100,000 species of sawflies, wasps, ants and bees. Hymenop-tera exhibit haplodiploid sex determination, where males arise from unfertilized haploid eggs and females arise from fertilized diploid eggs. Haplodiploid-induced asymmetries in relatedness between off-spring and sisters have long been thought to be involved in the evolution or maintenance of eusociality in the Hymenoptera 15,16 , but other life history traits also promote social evolution 17 , and there are divergent perspectives on this issue at the present time 1,18 . Haplodiploidy has distinct sex-determination mechanisms com-pared with other organisms because Hymenoptera lack sex chromosomes 19 . Hymenoptera is one of 11 orders of holometabolous (undergo a metamorphic moult) insects. All completed insect genome sequences have thus far been confined to Holometabola 20–26 ; phylogenetic rela-tionships of these and related arthropods are in Fig. 1. Honeybees diverged from Diptera and Lepidoptera 300 million years ago, whereas the last common ancestor with humans was 600 million years ago 27 . The genus Apis is an ancient lineage of bees that evolved in tropical Eurasia 28 and migrated north and west, reaching Europe by the end of the Pleistocene epoch, 10,000 yr ago. The origin of A. mellifera has been suggested as Asia 28 , the Middle East 29 , or Africa 2,30 . From there, humans carried them worldwide because of their ability to make honey 28 . The A. mellifera genome has novel characteristics and provides fascinating insights into honeybee biology. Some main findings are:

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    • "The divergence times (the evolutionary distances in time between each species and the common ancestor with its neighbour in this figure) are given as horizontal bars and are from data presented in [139] [162], or in the various relevant ''white papers'' accessible on the internet. The completed insect genomes are published in [1] [62] [111] [115] [133] [162] [166] (colors in this figure can only be seen in the online version of the article). brane, or 7TM receptors. "
    Dataset: TriboGPCRS

    Full-text · Dataset · Jan 2013
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    • "These studies stated that M and L receptors project to the first visual neuropil (the lamina; termination of the short visual fibers), while S receptors project to the second visual neuropil (the medulla; termination of the long visual fibers; Menzel and Blakers 1976; Meyer 1984). In the last 10 years, however, the advent of the honey bee genome (Honey Bee Genome Sequencing Consortium 2006) and the new molecular tools available have changed this view as they allowed studying photoreceptor distribution in the bee retina and their projections into the brain in a more precise way (Spaethe and Briscoe 2004, 2005; Velarde et al. 2005; Wakakuwa et al. 2005). "
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    ABSTRACT: The honey bee is a traditional animal model for the study of visual perception, learning, and memory. Extensive behavioral studies have shown that honey bees perceive, learn, and memorize colors, shapes, and patterns when these visual cues are paired with sucrose reward. Bee color vision is trichromatic, based on three photoreceptor types (S, M, L), which peak in the UV, blue, and green region of the spectrum. Perceptual color spaces have been proposed to account for bee color vision, and the anatomy of the visual neuropils in the bee brain was described to a large extent. In the last decade, conceptual and technical advances improved significantly our comprehension of visual processing in bees. At the behavioral level, unexpected cognitive visual capacities were discovered such as categorical and conceptual categorization. At the neurobiological level, molecular analyses of the compound eye revealed an intricate heterogeneity in the distribution of photoreceptors in the retina. Spatial segregation and integration of visual information in the bee brain has been analyzed at functional levels so far unexploited. These recent discoveries associated with the perspective of accessing the bee brain of harnessed bees while they perceive and learn visual cues open new avenues toward a comprehension of the neural substrates of visual perception and learning in bees. Understanding how the miniature brain of bees achieves sophisticated visual performances is a fundamental goal for the comparative study of vision and cognition.
    Full-text · Article · May 2012 · Apidologie
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    • "Functional insights into differentially expressed genes (all > two fold up/downregulated genes [P < 0.01]) were obtained by conducting a GO term enrichment analysis. We performed this analysis using the FlyBase identification number representing the best BLAST hit for each honey bee gene (Honey bee Genome Sequencing Consortium 2006). Enrichment in GO terms of biological processes on level 5 (GOTERM_BP5 chart) was determined by using GOToolBox (Martin et al. 2004) with a hypergeometric test followed by FDR correction for multiple testing (GO categories at P < 0.05 are shown). "
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    ABSTRACT: The honey bee is a major insect used for pollination of many commercial crops worldwide. Although the use of honey bees for pollination can disrupt the habitat, the effects on their physiology have never been determined. Recently, honey bee colonies have often collapsed when introduced in greenhouses for pollination in Japan. Thus, suppressing colony collapses and maintaining the number of worker bees in the colonies is essential for successful long-term pollination in greenhouses and recycling of honey bee colonies. To understand the physiological states of honey bees used for long-term pollination in greenhouses, we characterized their gene expression profiles by microarray. We found that the greenhouse environment changes the gene expression profiles and induces immune-suppression and oxidative stress in honey bees. In fact, the increase of the number of Nosema microsporidia and protein carbonyl content was observed in honey bees during pollination in greenhouses. Thus, honey bee colonies are likely to collapse during pollination in greenhouses when heavily infested with pathogens. Degradation of honey bee habitat by changing the outside environment of the colony, during pollination services for example, imposes negative impacts on honey bees. Thus, worldwide use of honey bees for crop pollination in general could be one of reasons for the decline of managed honey bee colonies.
    Full-text · Article · Oct 2011 · Ecology and Evolution
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