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Genetic control and evolution of sexually dimorphic characters in Drosophila

A Corrigendum to this article was published on 29 March 2001

Abstract

Sexually dimorphic abdominal pigmentation and segment morphology evolved recently in the melanogaster species group of the fruitfly Drosophila . Here we show that these traits are controlled by the bric-a-brac (bab) gene, which integrates regulatory inputs from the homeotic and sex-determination pathways. bab expression is modulated segment- and sex-specifically in sexually dimorphic species, but is uniform in sexually monomorphic species. We suggest that bab has an ancestral homeotic function, and that regulatory changes at the bab locus played a key role in the evolution of sexual dimorphism. Pigmentation patterns specified by bab affect mating preferences, suggesting that sexual selection has contributed to the evolution of bab regulation.

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Figure 1: Sexually dimorphic pigmentation is of recent evolutionary origin.
Figure 2: Control of male-specific pigmentation by Abd-B, dsx and bab.
Figure 3: Regulation of bab expression by Abd-B and dsx.
Figure 4: Repression of bab correlates with the presence of male-specific pigmentation.
Figure 5: Modulation of bab expression correlates with sexual dimorphism.
Figure 6: The homeotic function of bab.

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References

  1. Warren, R., Nagy, L., Selegue, J., Gates, J. & Carroll, S. Evolution of homeotic gene regulation and function in flies and butterflies. Nature 372, 458– 461 (1994).

    Article  ADS  CAS  Google Scholar 

  2. Burke, A. C., Nelson, C. E., Morgan, B. A. & Tabin, C. Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346 (1995).

    CAS  PubMed  Google Scholar 

  3. Averof, M. & Akam, M. Hox genes and the diversification of insect-crustacean body plans. Nature 376, 420–423 (1995).

    Article  ADS  CAS  Google Scholar 

  4. Brakefield, P. M. et al. Development, plasticity and evolution of butterfly eyespot patterns. Nature 384, 236– 242 (1996).

    Article  ADS  CAS  Google Scholar 

  5. Averof, M. & Patel, N. H. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388, 682–686 (1997).

    Article  ADS  CAS  Google Scholar 

  6. Stern, D. L. A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396, 463– 466 (1998).

    Article  ADS  CAS  Google Scholar 

  7. Sucena, E. & Stern, D. L. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc. Natl Acad. Sci. USA 97, 4530–4534 ( 2000).

    Article  ADS  CAS  Google Scholar 

  8. True, J. R., Stam, L. F., Zeng, Z. -B. & Laurie, C. C. Quantitative genetic analysis of divergence in male secondary sexual traits between Drosophila simulans and Drosophila mauritiana. Evolution 51, 816–832 ( 1997).

    Article  Google Scholar 

  9. Gurganus, M. C., Nuzhdin, S. V., Leips, J. W. & MacKay, T. F. High-resolution mapping of quantitative trait loci for sternopleural bristle number in Drosophila melanogaster. Genetics 152, 1535–1604 (1999).

    Google Scholar 

  10. Lyman, R. F., Lai, C. & MacKay, T. F. Linkage disequilibrium mapping of molecular polymorphisms at the scabrous locus associated with naturally occurring variation in bristle number in Drosophila melanogaster. Genet. Res. 74, 303–311 ( 1999).

    Article  CAS  Google Scholar 

  11. Anderson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).

    Google Scholar 

  12. Eberhard, W. G. Copulatory courtship and cryptic female choice in insects. Biol. Rev. 66, 1–31 ( 1991).

    Article  Google Scholar 

  13. Kopp, A. & Duncan, I. Control of cell fate and polarity in the adult abdominal segments of Drosophila by optomotor-blind . Development 124, 3703– 3714 (1997).

    CAS  PubMed  Google Scholar 

  14. Sanchez-Herrero, E., Vernos, I., Marco, R. & Morata, G. Genetic organization of the Drosophila bithorax complex. Nature 313, 108–113 (1985).

    Article  ADS  CAS  Google Scholar 

  15. Duncan, I. M. The bithorax complex. Annu. Rev. Genet. 21, 285–319 (1987).

    Article  CAS  Google Scholar 

  16. Celniker, S. E., Sharma, S., Keelan, D. J. & Lewis, E. B. The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J. 9, 4277–4286 (1990).

    Article  CAS  Google Scholar 

  17. Crosby, M. A., Lundquist, E. A., Tautvydas, R. M. & Johnson, J. The 3′ regulatory region of the Abdominal-B gene: genetic analysis supports a model of reiterated and interchangeable regulatory elements. Genetics 134, 809–824 ( 1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Hopmann, R., Duncan, D. & Duncan, I. Transvection in the iab-5,6,7 region of the bithorax complex of Drosophila: homology independent interactions in trans . Genetics 139, 815– 833 (1994).

    Google Scholar 

  19. Baker, B. S. & Ridge, K. A. Sex and the single cell. I. On the action of major loci affecting cell determination in Drosophila melanogaster . Genetics 94, 383– 423 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Cline, T. W. & Meyer, B. J. Vive al difference: males vs. females in flies vs. worms. Annu. Rev. Genet. 30, 637–702 (1996).

    Article  CAS  Google Scholar 

  21. McKeown, M. Sex differentiation: the role of alternative splicing. Curr. Opin. Genet. Dev. 2, 299–303 ( 1992).

    Article  CAS  Google Scholar 

  22. Burtis, K. C. The regulation of sex determination and sexually dimorphic differentiation in Drosophila. Curr. Opin. Cell Biol. 5, 1006–1014 (1993).

    Article  CAS  Google Scholar 

  23. Jursnich, V. A. & Burtis, K. C. A positive role in differentiation for the male doublesex protein of Drosophila. Dev. Biol. 155, 235–249 (1993).

    Article  CAS  Google Scholar 

  24. Waterbury, J. A., Jackson, L. L. & Schedl, P. Analysis of the doublesex female protein in Drosophila melanogaster: Role in sexual differentiation and behavior and dependence on intersex. Genetics 152, 1653– 1667 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Robertson, A., Briscoe, D. A. & Louw, J. H. Variation in abdomen pigmentation in Drosophila melanogaster females. Genetica 47, 73 –76 (1977).

    Article  Google Scholar 

  26. Godt, D., Couderc, J. -L., Cramton, S. E. & Laski, F. Pattern formation in the limbs of Drosophila: bric a brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus. Development 119, 799–812 (1993).

    CAS  PubMed  Google Scholar 

  27. Pointud, J. C. Fly base personal communications report 〈http://flybase.bio.indiana.edu/.bin/fbpcq.html?FBrf0104845〉 (1998).

  28. Nagoshi, R. N. & Baker, B. S. Regulation of sex-specific RNA splicing at the Drosophila doublesex gene: cis -acting mutations in exon sequences alter sex-specific RNA splicing patterns. Genes Dev. 4, 89–97 (1990).

    Article  CAS  Google Scholar 

  29. Burtis, K. C., Coschigano, K. T., Baker, B. S. & Wensink, P. C. The Doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 10, 2577–2582 (1991).

    Article  CAS  Google Scholar 

  30. Coshigano, K. T. & Wensink, P. C. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev. 7, 42– 54 (1993).

    Article  Google Scholar 

  31. Bock, I. R. Taxonomy of the Drosophila bipectinata species complex. Univ. Texas Publ. 7103, 273–280 (1971).

    Google Scholar 

  32. Ohnishi, S. & Watanabe, T. K. Genetic analysis of color dimorphism in the Drosophila montium subgroup. Jpn J. Genet. 60, 355–358 (1985).

    Article  Google Scholar 

  33. Fisher, R. A. The Genetical Theory Of Natural Selection (Dover, New York, 1958).

    MATH  Google Scholar 

  34. Carson, H. L. in Ecological Genetics: The Interface (ed. Brussard, P. F.) 93– 107 (Springer, New York, 1978).

    Book  Google Scholar 

  35. Lande, R. Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721– 3725 (1981).

    Article  ADS  MathSciNet  CAS  Google Scholar 

  36. Kirkpatrick, M. Sexual selection and the evolution of female choice. Evolution 36, 1–12 (1982 ).

    Article  Google Scholar 

  37. Carson, H. L. in Evolutionary Genetics (eds Singh, R. S. & Krimbas, C. B.) 495–512 (Cambridge Univ. Press, Cambridge, 1999).

    Google Scholar 

  38. Holland, B. & Rice, W. R. Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52, 1–7 (1998).

    Article  Google Scholar 

  39. Cordts, R. & Partridge, L. Courtship reduces longevity of male Drosophila melanogaster. Anim. Behav. 52, 269–278 (1996).

    Article  Google Scholar 

  40. Kopp, A. & Duncan, I. Technical tips for analyzing gene expression in the pupal abdomen. Dros. Info. Serv. (in the press).

  41. Bender, W. & Hudson, A. P element homing to the Drosophila bithorax complex. Development 127, 3981–3992 (2000).

    CAS  PubMed  Google Scholar 

  42. Kellerman, K. A. Mutations affecting the stability of the fushi tarazu protein of Drosophila. Genes Dev. 4, 1936– 1950 (1990).

    Article  CAS  Google Scholar 

  43. Bock, I. R. & Wheeler, M. R. The Drosophila melanogaster species group. Univ. Texax Publ. 7213, 1–102 (1972).

    Google Scholar 

  44. Bock, I. R. Current status of the Drosophila melanogaster species-group (Diptera). Syst. Entomol. 5, 341– 356 (1980).

    Article  Google Scholar 

  45. Pelandakis, M. & Solignac, M. Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J. Mol. Evol. 37, 525–543 ( 1993).

    Article  ADS  CAS  Google Scholar 

  46. Toda, M. J. Drosophilidae (Diptera) in Myanmar (Burma). VII. The Drosophila melanogaster species-group, excepting the D. montium species-subgroup. Orient. Insects 25, 69–94 (1991).

    Article  Google Scholar 

  47. Russo, C. A. M., Takezaki, N. & Nei, M. Molecular phylogeny and divergence times of drosophilid species. Mol. Biol. Evol. 12, 391– 404 (1995).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank F. Laski for bab stocks and antibodies; D. Godt for UAS- bab lines; W. Bender, S. Celniker and E. Sanchez-Herrero for the Abd-B enhancer trap and antibodies; J. David, Y. Fuyama, M. Kimura, J. Roote and the Bowling Green stock centre for various Drosophila species; L. Olds for the artwork; B. Holland, S. Nuzhdin, M. Servedio and J. True and T. Wittkopp for discussions. A.K. is a Howard Hughes Medical Institute fellow of the Life Sciences Research Foundation; I.D. is supported by an NIH grant; S.B.C. is an investigator at the Howard Hughes Medical Institute.

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Correspondence to Sean B. Carroll.

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Kopp, A., Duncan, I. & Carroll, S. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408, 553–559 (2000). https://doi.org/10.1038/35046017

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