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Genetica

, Volume 129, Issue 1, pp 37–43 | Cite as

Maternal expression increases the rate of bicoid evolution by relaxing selective constraint

  • Jeffery P. DemuthEmail author
  • Michael J. Wade
Original Paper

Abstract

Population genetic theory predicts that maternal effect genes will evolve differently than genes expressed in both sexes because selection is only half as effective on autosomal genes expressed in one sex but not the other. Here, we use sequences of the tandem gene duplicates, bicoid (bcd) and zerknüllt (zen), to test the prediction that, with similar coefficients of purifying selection, a maternal effect gene evolves more rapidly than a zygotic gene because of this reduction in selective constraint. We find that the maternal effect gene, bcd, is evolving more rapidly than zygotically expressed, zen, providing the first direct confirmation of this prediction of maternal effect theory from molecular evidence. Our results extend current explanations for the accelerated rate of bcd evolution by providing an evolutionary mechanism, relaxed selective constraint, that allows bcd the evolutionary flexibility to escape the typical functional constraints of early developmental genes. We discuss general implications of our findings for the role of maternal effect genes in early developmental patterning.

Keywords

Maternal effect genes bicoid zerknüllt Hox genes Developmental hourglass Molecular evolution Selective constraint 

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Notes

Acknowledgements

Our thanks to: C. Hughes, M. Lynch, and E. Brodie III, for insightful critiques and discussion of the manuscript. JPD was supported by a National Science Foundation—Integrated Graduate Education and Research Traineeship in Evolution, Development, and Genomics #9972830, and Doctoral Dissertation Improvement Grant #0206628. MJW and JPD were supported by the National Institutes of Health under Grant GM065414-01A.

References

  1. Barker MS, Demuth JP, Wade MJ (2005) Maternal expression relaxes constraint on innovation of the anterior determinant, bicoid. PLoS Genetics 1:e57PubMedCrossRefGoogle Scholar
  2. Binida-Emons ORP, Jeffrey JE, Richardson MK (2003) Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development. Proc R Soc Lond B 270:341–346CrossRefGoogle Scholar
  3. Dearden P, Akam M (1999) Developmental evolution: axial patterning in insects. Curr Biol 9:R591–R594PubMedCrossRefGoogle Scholar
  4. Dearden P, Grbic M, Falciani F, Akam M (2000) Maternal expression and early zygotic regulation of the Hox3/zen gene in the grasshopper Schistocerca gregaria. Evol Dev 2:261–270PubMedCrossRefGoogle Scholar
  5. Duboule D (1994) Temporal colinearity and the phylotypic progression—a basis for the stability of a vertebrate bauplan and the evolution of morphologies through heterochrony. Development Suppl. S:135–142Google Scholar
  6. Falciani F, Hausdorf B, Schroder R, Akam M, Tautz D, Denell R, Brown S (1996) Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci USA 93:8479–8484PubMedCrossRefGoogle Scholar
  7. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  8. Hughes AL (1999) Adaptive evolution of genes and genomes. Oxford University Press, New YorkGoogle Scholar
  9. Hughes CL, Kaufman TC (2002a) Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. Development 129:1225–1238Google Scholar
  10. Hughes CL, Kaufman TC (2002b) Hox genes and the evolution of the arthropod body plan. Evol Dev 4:459–499CrossRefGoogle Scholar
  11. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245PubMedCrossRefGoogle Scholar
  12. Kimura M (1962) On the probability of fixation of mutant genes in a population. Genetics 47:713–719PubMedGoogle Scholar
  13. Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New YorkGoogle Scholar
  14. Li W-H (1997) Molecular evolution. Sinauer Associates, Inc., Sunderland, MAGoogle Scholar
  15. Mousseau TA, Fox CW (eds) (1998) Maternal effects as adaptations. Oxford University Press, NYGoogle Scholar
  16. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, NYGoogle Scholar
  17. Raff RA (1996) The shape of life: genes, development, and the evolution of animal form. The University of Chicago Press, Chicago, ILGoogle Scholar
  18. Schröder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422:621–625PubMedCrossRefGoogle Scholar
  19. Stauber M, Jackle H, Schmidt-Ott U (1999) The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci USA 96:3786–3789PubMedCrossRefGoogle Scholar
  20. Stauber M, Taubert H, Schmidt-Ott U (2000) Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae). Proc Natl Acad Sci USA 97:10844–10849PubMedCrossRefGoogle Scholar
  21. Stauber M, Prell A, Schmidt-Ott U (2002) A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-cyclorrhaphan flies. Proc Natl Acad Sci USA 99:274–279PubMedCrossRefGoogle Scholar
  22. Thompson JD, Gibson TJ, Plenwniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882CrossRefGoogle Scholar
  23. Wade MJ (1998) The evolutionary genetics of maternal effects. In: Mosseau T, Fox C (eds) Maternal effects. Oxford University Press, Oxford, pp 5–21Google Scholar
  24. Wade MJ (2002) A gene’s eye view of epistasis, selection and speciation. J Evol Biol 15:337–346CrossRefGoogle Scholar
  25. Wade MJ (2002) The evolutionary genetics of maternal effects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, NY, pp 5–21Google Scholar
  26. Wade MJ, Beeman RW (1994) The population-dynamics of maternal-effect selfish genes. Genetics 138:1309–1314PubMedGoogle Scholar
  27. Whitlock MC, Wade MJ (1995) Speciation—founder events and their effects on X-linked and autosomal genes. Am Natur 145:676–685CrossRefGoogle Scholar
  28. Wolpert L, Beddington R, Jessell T, Lawrence P, Meyerowitz E, Smith J (2002) Principles of development. Oxford University Press, NYGoogle Scholar
  29. Wright S (1969) Evolution and the genetics of populations: vol 2, The theory of gene frequencies. The University of Chicago Press, Chicago, ILGoogle Scholar
  30. Zhang J, Rosenberg HF, Nei M (1998) Positive darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95:3708–3713PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA

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