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The function and evolution of a genetic switch controlling sexually dimorphic eye differentiation in honeybees

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  • Oksana Netschitailo

    (Heinrich-Heine University)

  • Yidong Wang

    (Wageningen University)

  • Anna Wagner

    (Heinrich-Heine University)

  • Vivien Sommer

    (Heinrich-Heine University)

  • Eveline C. Verhulst

    (Wageningen University)

  • Martin Beye

    (Heinrich-Heine University)

Abstract

Animals develop sex-specific morphological structures that are diverse between organisms. However, understanding the developmental and evolutionary mechanisms governing these traits is still limited and largely restricted to DM domain genes, which are conserved, sex-specific developmental regulators identified in genetic models. Here, we report a sex-specific developmental regulator gene, glubschauge (glu) that selectively regulates sexually dimorphic eye differentiation in honeybees. We found that the sex determination gene feminizer (fem) controls sex-specific splicing of glu transcripts, establishing a genetic switch in which Glu proteins with a zinc finger (ZnF) domain are only expressed in females. We showed that female coding sequence was essential and sufficient for partial feminization. Comparative sequence and functional studies revealed that the evolutionary origination of the genetic switch was followed by the mutational origin of the essential ZnF domain. Our results demonstrate that glu is a newly evolved sex-specific genetic switch for region-specific regulation of a dimorphic character.

Suggested Citation

  • Oksana Netschitailo & Yidong Wang & Anna Wagner & Vivien Sommer & Eveline C. Verhulst & Martin Beye, 2023. "The function and evolution of a genetic switch controlling sexually dimorphic eye differentiation in honeybees," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36153-4
    DOI: 10.1038/s41467-023-36153-4
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    1. Artyom Kopp & Ian Duncan & Sean B. Carroll, 2000. "Genetic control and evolution of sexually dimorphic characters in Drosophila," Nature, Nature, vol. 408(6812), pages 553-559, November.
    2. Christopher S. Raymond & Caroline E. Shamu & Michael M. Shen & Kelly J. Seifert & Betsy Hirsch & Jonathan Hodgkin & David Zarkower, 1998. "Evidence for evolutionary conservation of sex-determining genes," Nature, Nature, vol. 391(6668), pages 691-695, February.
    3. Jennifer L. Mummery-Widmer & Masakazu Yamazaki & Thomas Stoeger & Maria Novatchkova & Sheetal Bhalerao & Doris Chen & Georg Dietzl & Barry J. Dickson & Juergen A. Knoblich, 2009. "Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi," Nature, Nature, vol. 458(7241), pages 987-992, April.
    4. Bruno Hudry & Sanjay Khadayate & Irene Miguel-Aliaga, 2016. "The sexual identity of adult intestinal stem cells controls organ size and plasticity," Nature, Nature, vol. 530(7590), pages 344-348, February.
    5. Martin Hasselmann & Tanja Gempe & Morten Schiøtt & Carlos Gustavo Nunes-Silva & Marianne Otte & Martin Beye, 2008. "Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees," Nature, Nature, vol. 454(7203), pages 519-522, July.
    6. Frank Schnorrer & Cornelia Schönbauer & Christoph C. H. Langer & Georg Dietzl & Maria Novatchkova & Katharina Schernhuber & Michaela Fellner & Anna Azaryan & Martin Radolf & Alexander Stark & Krystyna, 2010. "Systematic genetic analysis of muscle morphogenesis and function in Drosophila," Nature, Nature, vol. 464(7286), pages 287-291, March.
    7. Benjamin Prud'homme & Nicolas Gompel & Antonis Rokas & Victoria A. Kassner & Thomas M. Williams & Shu-Dan Yeh & John R. True & Sean B. Carroll, 2006. "Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene," Nature, Nature, vol. 440(7087), pages 1050-1053, April.
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