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Wednesday, March 21, 2012

Honeybee Castes and Altruism

In honeybees the queen and the worker are both females, but the queen has a larger body size than the worker and produces abundant offspring. By contrast, the worker bees are effectively sterile and take care of the queen and her offspring. Whether a female becomes a queen or a worker is determined by the amount of royal jelly provided during embryogenesis. If the amount of royal jelly is high, a queen is produced, but otherwise a worker bee is born. In a recent Nature paper, Kamakura (1) showed that royal jelly contains the protein Royalactin and this protein initiates the development of a queen. Therefore, the presence or absence of this protein generates the castes of the queen and the worker. In a “News and Comments” paper in Nature, Gene Robinson (2) praised this paper stating that Kamakura solved a 100-year old problem. Because the detail of Kamakura’s molecular study is explained by Robinson, I refer the reader to his article as well as Kamakura’s original paper.
In this commentary, I would like to discuss other aspects of evolution of castes and altruism. As is well known, Bill Hamilton (3) published a mathematical paper deriving the condition of evolution of different castes or eusociality. Some time ago, I tried to read the paper, but I was not happy with his formulation. Recently, Nowak, Tarnita, and Wilson (4) re-examined Hamilton’s theoretical work and rejected it. This paper then received hostile responses from the sociobiology community including the five papers simultaneously published in Nature. However, Nowak et al. does not give up their criticism (5). They believe that the caste system in hymenopteran insects has evolved by group selection, as Charles Darwin speculated, and propose one evolutionary scenario of eusociality.
In my view, this problem should be studied by using the molecular approach rather than the mathematical. Kamakura’s study indicates that eusociality can evolve irrespective of haplodiploid or diplodiploid sex determination, because he showed that the ectopic expression of royalactin produces a queen-like female even in Drosophila. This indicates that differentiation of the queen and the worker is initiated by one or a few genes. This finding questions the validity of Hamiliton's principle. The molecular biology of behavioral characters has been studied extensively for more than 40 years after Seymour Benzer’s pioneering work. Of course, the evolution of eusociality is quite complicated compared with the characters studied by molecular biologists. However, it is encouraging that several groups of evolutionists are now working on this subject using various insect species (e.g. 6, 7, 8, 9, 10).
             It is now known that many genes controlling sex determination and eusociality are shared by different insect species, and the expression of several genes is controlled by alternative splicing. For example, the feminizer (fem) gene that initiates the formation of female phenotype in honeybees is orthologous to the transformer (tra) gene in medfly, housefly, and Drosophila, and multiple splicing is necessary for these genes to produce functional proteins.

1. Kamakura M. 2011. Royalactin induces queen differentiation in honeybees. Nature 473:478-483.
2. Robinson G. 2011. Royal aspirations. Nature 473:454-455.
3. Hamilton WD. 1964. The genetical evolution of social behavior, I and II. J Theor Biol 7:1-52.
4. Nowak MA, Tarnita CE, and Wilson EO. 2010. The evolution of eusociality. Nature 466:1057-1062.
5. Nowak MA, Tarnita CE, and Wilson EO. 2011. Nowak et al. reply. Nature 471:E9-E10.
7. Rajakumar R, San Mauro D, Dijkstra MB, Huang MH, Wheeler DE, Hiou-Tim F, Khila A, Cournoyea M, and Abouheif E. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335:79-82.
8. Hasselmann M, Gempe T, Nunes-Silva CG, Otte M, Beye M. 2008. Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454: 519-522.
9. Verhulst EC, Beukeboom LW, van de Zande L. 2010. Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328:620-3.
10. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, and Maleszka R. 2012. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. PNAS Early Edition.