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Originally published as Genetics Published Articles Ahead of Print on October 18, 2007.

Genetics, Vol. 177, 1733-1741, November 2007, Copyright © 2007
doi:10.1534/genetics.107.078980

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Sex-Specific Splicing of the Honeybee doublesex Gene Reveals 300 Million Years of Evolution at the Bottom of the Insect Sex-Determination Pathway

Soochin Cho*, Zachary Y. Huang{dagger} and Jianzhi Zhang*,1

* Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109 and {dagger} Department of Entomology, Michigan State University, East Lansing, Michigan 48824

1 Corresponding author: Department of Ecology and Evolutionary Biology, University of Michigan, 1075 Natural Science Bldg., 830 North University Ave., Ann Arbor, MI 48109.
E-mail: jianzhi{at}umich.edu

Sex-determination mechanisms vary greatly among taxa. It has been proposed that genetic sex-determination pathways evolve in reverse order from the final step in the pathway to the first step. Consistent with this hypothesis, doublesex (dsx), the most downstream gene in the Drosophila sex-determination cascade that determines most sexual phenotypes also determines sex in other dipterans and the silk moth, while the upstream genes vary among these species. However, it is unknown when dsx was recruited to the sex-determination pathway during insect evolution. Furthermore, sex-specific splicing of dsx, by which dsx determines sex, is different in pattern and mechanism between the moth and the fly, raising an interesting question of how these insects have kept the executor of sex determination while allowing flexibility in the means of execution. To address these questions, here we study the dsx gene of the honeybee Apis mellifera, a member of the most basal lineage of holometabolous insects. We report that honeybee dsx is sex-specifically spliced and that it produces both the fly-type and moth-type splicing forms, indicating that the use of different splicing forms of Dsx in controlling sexual differentiation was present in the common ancestor of holometabolous insects. Our data suggest that in ancestral holometabolous insects the female Dsx form is the default and the male form is generated by suppressing the splicing of the female form. Thus, it is likely that the dsx splicing activator system in flies, where the male form is the default, arose during early dipteran evolution.


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Copyright © 2007 by the Genetics Society of America.