Genetic control and evolution of sexually dimorphic characters in Drosophila

Article metrics

  • 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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 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).

  2. 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).

  3. 3

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

  4. 4

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

  5. 5

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

  6. 6

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

  7. 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).

  8. 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).

  9. 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).

  10. 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).

  11. 11

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

  12. 12

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

  13. 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).

  14. 14

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

  15. 15

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

  16. 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).

  17. 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).

  18. 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).

  19. 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).

  20. 20

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

  21. 21

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

  22. 22

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

  23. 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).

  24. 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).

  25. 25

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

  26. 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).

  27. 27

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

  28. 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).

  29. 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).

  30. 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).

  31. 31

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

  32. 32

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

  33. 33

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

  34. 34

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

  35. 35

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

  36. 36

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

  37. 37

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

  38. 38

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

  39. 39

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

  40. 40

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

  41. 41

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

  42. 42

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

  43. 43

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

  44. 44

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

  45. 45

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

  46. 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).

  47. 47

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

Download references

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.

Author information

Correspondence to Sean B. Carroll.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.