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Honey Bee - Beye

Sweet yet sophisticated: The honey bee genome lends insight into sociality, sensation, and sex

Genome Research has devoted this month’s issue to studies that provide insight into the biology of the honey bee (Apis mellifera). The issue will appear online and in print on October 26, concomitant with the publication of the honey bee genome sequence in the journal Nature.

1. On the fast track to evolutionary complexity

Since its split from the bumble bee 60 million years ago, the honey bee has evolved the highest rate of recombination—the process by which genetic material is physically mixed during sexual reproduction—of any known animal. In their Genome Research article, Dr. Martin Beye and his colleagues relate the sequence features of the honey bee genome to this strikingly high recombination rate.

Beye’s team found an average of 5.7 chiasmata (crossovers) per chromosome in honey bees, while closely related species (bumble bees and parasitic wasps) as well as more distantly related species (fruit flies, worms, and humans) exhibited, on average, only 1.6 chiasmata per chromosome. The researchers dismiss the copious crossovers as necessary for stabilizing the chromosomes and, instead, propose an evolutionary theory to account for their findings.

“The honey bee has a small breeding population because the queen is the only reproductive female in the colony,” explains Beye. “The increased recombination rate boosts the genetic diversity in the honey bee population, which in turn speeds the evolution of more selectively advantageous traits. This could help slow the spread of parasites in colonies, for example, or provide a basis for task specialization, leading to an increase in social complexity, colony performance, and fitness.”

Contact: Martin Beye, Ph.D.
Heinrich Heine Universität Düsseldorf, Germany

Beye, M., et al. 2006. Exceptionally high levels of recombination across the honey bee genome. Genome Res. 16: 1339-1344. [DOI: 10.1101/gr.5680406]

2. The genealogy of the royal (protein) lineage

In honey bees, the queens are not of royal blood, but royal jelly: they become sexually mature only after being chosen by workers from the previous generation to perpetually receive royal jelly, a viscous substance rich in proteins, lipids, vitamins, and other nutrients. Approximately 90% of proteins in royal jelly are from the Major Royal Jelly Protein (MRJP) gene family. In the current issue of Genome Research, a team of scientists led by Dr. Ryszard Maleszka used the honey bee genome sequence to perform a comprehensive analysis of the evolution, genomic organization, and presumed function of the MRJPs.

Maleszka’s team demonstrated that MRJP genes, found only in honey bees and closely related hymenopteran insects, were derived from an ancient family of genes in bacteria that produce Yellow proteins. But while protein products of the MRJP and Yellow genes shared extensive sequence similarities, they exhibited diverse expression patterns, indicating divergent physiological functions.

“Our work indicates that MRJPs perform context-dependent functions,” explains Maleszka. “The proteins expressed in the brain or during development will have different phenotypic implications than those consumed as nutrients in royal jelly. In honey bees, nature and nurture converge to determine complex behavior.”

Ryszard Maleszka, Ph.D.
The Australian National University

Drapeau, M.D., Albert, S., Kucharski, R., Prusko, C., and Maleszka, R. 2006. Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honeybees. Genome Res. 16: 1385-1394. [DOI: 10.1101/gr.5012006]

3. Smelling out genes for chemical detection

Honey bees live in a chemical world; their survival depends on their ability to detect floral scents and communicate via pheromones with other bees in the hive. Discrimination among various chemical cues involves specific nerve cell receptors for smell (olfaction) and taste (gustation). With the genome sequence of the honey bee now in hand, Drs. Hugh Robertson and Kevin Wanner have identified the complete repertoire of receptors responsible for capturing these cues.

In their Genome Research article, Robertson and Wanner report the identification of 163 olfactory receptors, which is more than twice the number in fruit flies (62) and mosquitoes (79). “The expansion of olfactory receptors in bees underlies their social complexity and skill at locating flowers,” explains Robertson.

On the other hand, the scientists identified only 10 gustatory receptor genes in the honey bee genome, far fewer than in fruit fly (68) or mosquito (76). “Bees have little need for gustatory receptors to locate and recognize food,” Robertson says. “The larvae are sequestered in cells in the hive and are provisioned by adult nurse bees. And flowering plants have evolved mechanisms to attract and reward bees for pollination services, so there was little need for the bees to develop additional taste receptors.”

Hugh M. Robertson, Ph.D.
University of Illinois, Urbana-Champaign

Robertson, H.M. and Wanner, K.W. 2006. The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family. Genome Res. 16: 1395-1404. [DOI: 10.1101/gr.5057506]

4. Dancing to the beat of a mammalian drummer

In honey bees, the circadian clock is involved in several complex behaviors, including time sensing, navigation, labor division, and their famous dance language. The molecular basis of the circadian clock involves several interlocked pathways and associated regulatory components. Using the honey bee genome sequence, a team of researchers led by Dr. Guy Bloch has identified and characterized the core set of genes responsible for circadian rhythms in honey bees.

As described in Genome Research, Bloch’s group found that the composition and expression patterns of clock genes in the honey bee genome were more similar to the mammalian model (mouse) than to the insect model (fruit fly). “These results raise several questions on the evolution and function of animal clocks,” says Bloch. “How was the clock of ancient animals organized? What is the functional significance of genetic variation in the molecular clockwork?”

While these questions may not be answered until the circadian clocks of additional organisms are characterized at the molecular level, it is interesting to note the similarities in the clockwork of honey bees and mammals—and to consider how these similarities may be linked to the development of complex behavior in these organisms. The current study paves the way for future molecular and biochemical analyses of circadian rhythms and complex behaviors in insects, humans, and other species.

Guy Bloch, Ph.D.
The Hebrew University of Jerusalem, Israel

Rubin, E., Shemesh, Y., Cohen, M., Elgavish, S., Robertson, H.M., and Bloch, G. 2006. Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res. 16: 1352-1365. [DOI: 10.1101/gr.5094806]

5. On sex and death

A honey bee’s sex is determined by the genotype of a single gene called csd (complementary sex determination). When honey bees inherit different combinations of csd variants, three outcomes are possible: hemizygotes (unfertilized eggs with only one copy of csd) become male, heterozygotes (with two different copies of csd) become female, and homozygotes (with two exact copies of csd) develop into males that are eaten by workers after they hatch.

Because the homozygotes do not survive to reproductive age, csd was theoretically expected to exhibit a high level of polymorphism in the honey bee population. In their Genome Research article, Dr. Jianzhi Zhang and colleagues provide experimental data showing that the polymorphic level of the csd gene is approximately seven times higher than neutral regions of the honey bee genome. Furthermore, many csd gene variants are shared among different Asian and Western honey bee species, indicating a selective advantage for maintaining the different gene variants in the population—the phenomenon that geneticists call “balancing selection.”

“Understanding the mode and mechanism of honey bee sex determination are instrumental for designing successful matings and developing bee-breeding technologies,” explains Zhang. “The new data and analyses of these csd genes provide useful resources for breeding these economically important insects.”

Jianzhi Zhang, Ph.D.
University of Michigan

Cho, S., et al. 2006. Evolution of the complementary sex-determination gene of honey bees: balancing selection and trans-species polymorphisms. Genome Res. 16: 1366-1375. [DOI: 10.1101/gr.4695306]

Please direct requests for pre-print copies of the manuscripts to Peggy Calicchia (calicchi@cshl.org; +1-516-422-4012), the Editorial Secretary for Genome Research. An electronic file (5” х 6.5”, 300 dpi, JPEG) of the cover for the Genome Research Honey Bee Genome issue is also available. In addition to those articles highlighted above, the following are also available:

6.Elsik, C.G., Worley, K.C., Zhang, L., Milshina, N.V., Jiang, H., Reese, J.T., Childs, K.L., Venkatraman, A., Dickens, C.M., Weinstock, G.M., and Gibbs, R.A. 2006. Community annotation: Procedures, protocols, and supporting tools. Genome Res. 16: 1329-1333. [DOI: 10.1101/gr.5580606]

7.Savard, J., Tautz, D., Richard, S., Weinstock, G.M., Gibbs, R.A., Werren, J.H., Tettelin, H., and Lercher, M.J. 2006. Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res. 16: 1334-1338. [DOI: 10.1101/gr.5204306]

8.Robertson, H.M. and Gordon, K.H.J. 2006. Canonical TTAGG-repeat telomeres and telomerase in the honey bee, Apis mellifera. Genome Res. 16: 1345-1351. [DOI: 10.1101/gr.5085606]

9.Dearden, P.K., Wilson, M.J., Sablan, L., Osborne, P.W., Havler, M., McNaughton, E., Kimura, K., Milshina, N.V., Hasselmann, M., Gempe, T., Schioett, M., Brown, S.J., Elsik, C.G., Holland, P.W.H., Kadowaki, T., and Beye, M. 2006. Patterns of conservation and change in honey bee developmental genes. Genome Res. 16: 1376-1384. [DOI: 10.1101/gr.5108606]

10.Forêt, S., and Maleszka, R. 2006. Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res. 16: 1404-1413. [DOI: 10.1101/gr.5075706]

11.Sutherland, T.D., Campbell, P.M., Weisman, S., Trueman, H.E., Sriskantha, A., Wanjura, W.J., and Haritos, V.S. 2006. A highly divergent gene cluster in honey bees encodes a novel silk family. Genome Res. 16: 1414-1421. [DOI: 10.1101/gr.5052606]

12.Jones, A.K., Raymond-Delpech, V., Thany, S.H., Gauthier, M., and Sattelle, D.B. 2006. The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res. 16: 1422-1430. [DOI: 10.1101/gr.4916306]

Genome Research (www.genome.org) is an international, monthly, peer-reviewed journal published by Cold Spring Harbor Laboratory Press. Launched in 1995, it is one of the five most highly cited primary research journals in genetics and genomics.

Cold Spring Harbor Laboratory Press is an internationally renowned publisher of books, journals, and electronic media located on Long Island, New York. It is a division of Cold Spring Harbor Laboratory, an innovator in life science research and the education of scientists, students, and the public. For more information, visit www.cshlpress.com.
Genome Research issues press releases to highlight significant research studies that are published in the journal.

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