title: Gradual molecular evolution of a sex determination switch through incomplete penetrance of femaleness.
abstract: Some genes regulate phenotypes that are either present or absent. They are often important regulators of developmental switches and are involved in morphological evolution. We have little understanding of the molecular mechanisms by which these absence/presence gene functions have evolved, because the phenotype and fitness of molecular intermediate forms are unknown. Here, we studied the sex-determining switch of 14 natural sequence variants of the csd gene among 76 genotypes of the honeybee (Apis mellifera). Heterozygous genotypes (different specificities) of the csd gene determine femaleness, while hemizygous genotypes (single specificity) determine maleness. Homozygous genotypes of the csd gene (same specificity) are lethal. We found that at least five amino acid differences and length variation between Csd specificities in the specifying domain (PSD) were sufficient to regularly induce femaleness. We estimated that, on average, six pairwise amino acid differences evolved under positive selection. We also identified a natural evolutionary intermediate that showed only three amino acid length differences in the PSD relative to its parental allele. This genotype showed an intermediate fitness because it implemented lethality regularly and induced femaleness infrequently (i.e., incomplete penetrance). We suggest incomplete penetrance as a mechanism through which new molecular switches can gradually and adaptively evolve.
authors: Institute of Evolutionary Genetics, Heinrich Heine University Duesseldorf, Universitaetsstrasse 1, 40225 Duesseldorf, Germany. Electronic address: martin.beye@hhu.de.
authors: Martin
authors: M
authors: Beye
authors: Institute of Evolutionary Genetics, Heinrich Heine University Duesseldorf, Universitaetsstrasse 1, 40225 Duesseldorf, Germany.
authors: Christine
authors: C
authors: Seelmann
authors: Institute of Evolutionary Genetics, Heinrich Heine University Duesseldorf, Universitaetsstrasse 1, 40225 Duesseldorf, Germany.
authors: Tanja
authors: T
authors: Gempe
authors: Institute of Genetics, University of Cologne, Zuelpicher Straße 47, 50674 Koeln, Germany.
authors: Martin
authors: M
authors: Hasselmann
authors: Laboratoire de Génétique et Evolution des Populations Végétales, UMR 8198, CNRS, Université Lille 1, 59655 Villeneuve d'Ascq, France.
authors: Xavier
authors: X
authors: Vekemans
authors: School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA.
authors: M Kim
authors: MK
authors: Fondrk
authors: School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA.
authors: Robert E
authors: RE
authors: Page
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001516:Bees / Q000235:genetics* / Q000254:growth & development; D019143:Evolution, Molecular; D005260:Female; D014644:Genetic Variation; D005838:Genotype; D019476:Insect Proteins / Q000737:chemistry / Q000235:genetics*; D008297:Male; D008969:Molecular Sequence Data; D016415:Sequence Alignment; D019849:Sex Determination Processes
chemical_list: D019476:Insect Proteins