The profound biological changes that lofted the honeybee to an advanced state of social organization are reflected in its newly sequenced genome. The species can now be studied all the way from molecule to colony.
The transformation of an insect species from a solitary lifestyle to advanced colonial existence requires alterations in every system of the body, coupled with sufficient plasticity in the traits prescribed by the genes to generate strong differences among the adult castes. A picture of this revolution at the genomic level is published in this issue (page 931)1.
If Earth's social organisms are scored by complexity of communication, division of labour and intensity of group integration, three pinnacles of evolution stand out: humanity, the jellyfish-like siphonophores, and a select assemblage of social insect species2,3. The honeybee, Apis mellifera, is a member of this insect group — which also includes the spectacular leaf-cutting ants, army ants and macrotermitine mound-building termites — and no one can deny that it belongs in this front rank4.
As pointed out by the paper's authors1, the abiding mystery of A. mellifera is how creatures as tiny as worker bees, with brains containing only a millionth the number of neurons as do ours, are able to perform so many tasks and integrate them into a harmonious whole. Since the first publication on honeybees of the modern era, Charles Butler's Feminine Monarchie (1609), discoveries have flowed at the organism and colony levels, justifying Karl von Frisch's remark that, to scientists, “The life of bees is like a magic well. The more you draw from it, the more there is to draw.”
The most celebrated characteristic of A. mellifera, next to its honey and pollination services, is, of course, the waggle dance. Foraging workers, on returning to the hive after successful searches for food sources or new nest sites, run figures-of-eight on the vertical comb surfaces, with the middle segment of their body symbolically representing the flight to be taken outward. This latter 'waggle run' contains information about the direction of the target with reference to the Sun, as well as conveying distance from the hive. Timed buzzing and odour secretion enhance the message. Circular 'round dances' supplant the full waggle dance to inform nestmates that the target is close to the nest.
Research in recent years has revealed other performances on the honeybee dance card. If the returning foragers discover many food handlers unemployed as they unload their harvest, they perform the 'shaking dance' to bring more workers on to the dance floor and thence out to the field. If the reverse occurs, in other words if the foragers have trouble passing on their load, they engage in 'tremble dances', to draft in more bees to act as food handlers.
In addition to their terpsichorean programme, honeybees employ pheromones. These substances, secreted from glands distributed over the body, variously alarm or recruit nestmates, distinguish them from alien bees, and classify them according to gender, caste and age4,5. As workers pass through their natural adult lifespan of about 40 days, their socially active glands variously grow and shrink in programmed time sequences in concert with the labour roles they assume6,7. The progression can be speeded up or reversed according to the needs of the colony8. And as they shift among specialities, their receptiveness to particular signals rises or falls.
Finally, worker bees possess an extraordinary memory capacity. They learn the odour of the colony to which they belong. On foraging flights, they use landmarks as well as the instructions given by their dancing nestmates. They can recall the location of up to five flower-beds or other food sites, together with the approximate time of day in which each is most productive8,9.
The decoders of the honeybee genome have begun to address these remarkable social traits at the molecular-genetic level (Box 1, overleaf). From work by generations of previous researchers, they were already aware that virtually every biological system has been altered to some degree. A first reading of the genome reveals, not unexpectedly, that some of the genes have been modified from ancient precursors. For example, a cluster descended from a single progenitor gene that encoded a member of the yellow protein family here prescribes the royal jelly used in caste determination and queen production. Others, including those that programme chemoreception and food management, seem to include innovations that have evolved since the bee lineage split from that of other insects.
This DNA sequence is a major step towards answering a basic question of social evolution: at the genomic level, what does it take to engineer an advanced colonial insect? As this work is extended, it will soon come to address a second, equally important question: what does it take to make a eusocial insect species in the first place? (In eusocial colonies, members comprise overlapping generations that are divided into reproductive and worker castes to care for the young.) Fortunately, a large fund of information can be gathered to settle this issue, because among the 16,000 or so living bee species known, some are solitary but close to the threshold of eusociality, others have barely made it across the threshold, a few have reverted back to the solitary state, and still others have settled at various degrees of social organization intermediate to the honeybee grade. The evolutionary histories of most of these lines have been worked out on the basis of anatomy10, and in a few cases with the aid of partial molecular evidence. Among those closest to the honeybees are the solitary euglossines, the bumblebees and the meli-ponine stingless bees, the last of which seem comparable in complexity of social organization to the honeybees.
As pieces of this great mosaic are put in place with the aid of comparative genomics, a remarkable history will emerge, yielding many perspectives in developmental evolution and sociobiology.
The Honeybee Genome Sequencing Consortium Nature 443, 931–949 (2006).
Wilson, E. O. Sociobiology: The New Synthesis (Harvard Univ. Press, 1975).
Choe, J. C. & Crespi, B. J. (eds) The Evolution of Social Behavior in Insects and Arachnids (Cambridge Univ. Press, 1997).
Seeley, T. D. The Wisdom of the Hive (Harvard Univ. Press, 1995).
Michener, C. D. The Social Behavior of the Bees: A Comparative Study (Harvard Univ. Press, 1974).
Sekiguchi, F. & Sakagami, S. F. Rep. Hokkaido Natl Agric. Exp. Sta. 69, 1–65 (1966).
Lindauer, M. Communication Among Social Bees (Harvard Univ. Press, 1961).
Rösch, G. A. Z. Vergl. Physiol. 12, 1–71 (1930).
von Frisch, K. The Dance Language and Orientation of Bees (Harvard Univ. Press, 1967).
Michener, C. D. The Bees of the World (Johns Hopkins Univ. Press, 2000).
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