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

Nature (Impact Factor: 38.6). 10/2006;

ABSTRACT 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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