Abstract
Little is known about broad patterns of variation and evolution of gene expression during any developmental process. Here we investigate variation in genome-wide gene expression among Drosophila simulans, Drosophila yakuba and four strains of Drosophila melanogaster during a major developmental transition—the start of metamorphosis. Differences in gene activity between these lineages follow a phylogenetic pattern, and 27% of all of the genes in these genomes differ in their developmental gene expression between at least two strains or species. We identify, on a gene-by-gene basis, the evolutionary forces that shape this variation and show that, both within the transcriptional network that controls metamorphosis and across the whole genome, the expression changes of transcription factor genes are relatively stable, whereas those of their downstream targets are more likely to have evolved. Our results demonstrate extensive evolution of developmental gene expression among closely related species.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
King, M.C. & Wilson, A.C. Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975).
Davidson, E.H. Genomic Regulatory Systems: Development and Evolution (Academic, San Diego, 2001).
Johnson, N.A. & Porter, A.H. Toward a new synthesis: population genetics and evolutionary developmental biology. Genetica 112, 45–58 (2001).
Wilkins, A.S. The Evolution of Developmental Pathways (Sinauer, New York, 2001).
Dickinson, W.J. On the architecture of regulatory systems—evolutionary insights and implications. BioEssays 8, 204–208 (1988).
Wagner, G.P. Homologues, natural kinds and the evolution of modularity. Am. Zool. 36, 36–43 (1996).
Dickinson, W.J., Yang, Y.F., Schuske, K. & Akam, M. Conservation of molecular prepatterns during the evolution of cuticle morphology in Drosophila larvae. Evolution 47, 1396–1406 (1993).
McGinnis, W., Garber, R.L., Wirz, J., Kuroiwa, A. & Gehring, W.J. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37, 403–408 (1984).
Alonso, C.R., Maxton-Kuechenmeister, J. & Akam, M. Evolution of Ftz protein function in insects. Curr. Biol. 11, 1473–1478 (2001).
Wimmer, E.A., Carleton, A., Harjes, P., Turner, T. & Desplan, C. bicoid-independent formation of thoracic segments in Drosophila. Science 287, 2476–2479 (2000).
Wagner, G.P. & Gauthier, J.A. 1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proc. Natl. Acad. Sci. USA 96, 5111–5116 (1999).
Wagner, G.P. & Misof, B.Y. How can a character be developmentally constrained despite variation in developmental pathways? J. Evol. Biol. 6, 449–455 (1993).
Palopoli, M.F., Davis, A.W. & Wu, C.I. Discord between the phylogenies inferred from molecular versus functional data: uneven rates of functional evolution or low levels of gene flow? Genetics 144, 1321–1328 (1996).
Reinke, V. & White, K. Developmental genomic approaches in model organisms. Annu. Rev. Genom. Hum. G. 3, 153–178 (2002).
Cavalieri, D., Townsend, J.P. & Hartl, D.L. Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis. Proc. Natl. Acad. Sci. USA 97, 12369–12374 (2000).
Hughes, T.R. et al. Functional discovery via a compendium of expression profiles. Cell 102, 109–126 (2000).
Damerval, C., Maurice, A., Josse, J.M. & Devienne, D. Quantitative trait loci underlying gene-product variation—a novel perspective for analyzing regulation of genome expression. Genetics 137, 289–301 (1994).
Jin, W. et al. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat. Genet. 29, 389–395 (2001).
Schena, M., Shalon, D., Davis, R.W. & Brown, P.O. Quantitative monitoring of gene-expression patterns with a complementary-DNA microarray. Science 270, 467–470 (1995).
Riddiford, L.M. in The Development of Drosophila melanogaster Vol. 2 (eds. Bate, M. & Arias, A.M.) 899–940 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1993).
White, K.P., Rifkin, S.A., Hurban, P. & Hogness, D.S. Microarray analysis of Drosophila development during metamorphosis. Science 286, 2179–2184 (1999).
Arbeitman, M.N. et al. Gene expression during the life cycle of Drosophila melanogaster. Science 297, 2270–2275 (2002).
Moriyama, E.N. & Powell, J.R. Intraspecific nuclear DNA variation in Drosophila. Mol. Biol. Evol. 13, 261–277 (1996).
Lachaise, D. et al. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22, 159–225 (1988).
Powell, J.R. Progress and Prospects in Evolutionary Biology. The Drosophila Model (Oxford Univ. Press, New York, 1997).
Kerr, M.K. et al. Statistical analysis of a gene expression microarray experiment with replication. Stat. Sin. 12, 203–217 (2002).
Lande, R. Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314–334 (1976).
Lynch, M. & Hill, W.G. Phenotypic evolution by neutral mutation. Evolution 40, 915–935 (1986).
Turelli, M., Gillespie, J.H. & Lande, R. Rate tests for selection on quantitative characters during macroevolution and microevolution. Evolution 42, 1085–1089 (1988).
Ashburner, M. Patterns of puffing activity in salivary gland chromosomes of Drosophila. 3. A comparison of autosomal puffing patterns of sibling species D. melanogaster and D. simulans. Chromosoma 27, 156–177 (1969).
Ashburner, M. & Lemeunie, F. Patterns of puffing activity in salivary-gland chromosomes of Drosophila.7. Homology of puffing patterns on chromosome arm 3L in D. melanogaster and D. yakuba, with notes on puffing in D. teissieri. Chromosoma 38, 283–295 (1972).
Wensink, P.C., Finnegan, D.J., Donelson, J.E. & Hogness, D.S. System for mapping DNA sequences in chromosomes of Drosophila melanogaster. Cell 3, 315–325 (1974).
Stowers, R.S., Russell, S. & Garza, D. The 82F late puff contains the L82 gene, an essential member of a novel gene family. Dev. Biol. 213, 116–130 (1999).
The Gene Ontology Consortium. The Gene Ontology: tool for the unification of biology. Nat. Genet. 25, 25–29 (2000).
Robertson, C.W. The metamorphosis of Drosophila melanogaster, including an accurately timed account of the principal morphological changes. J. Morphol. 59, 351–399 (1939).
Lewontin, R.C. The organism as the subject and object of evolution. Scientia 188, 65–82 (1983).
Toma, D.P., White, K.P., Hirsch, J. & Greenspan, R.J. Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nat. Genet. 31, 349–353 (2002).
White, K.P. Functional genomics and the study of development, variation, and evolution. Nat. Rev. Genet. 2, 528–537 (2001).
Maroni, G. & Stamey, S.C. Use of blue food to select synchronous late 3rd instar larvae. Drosoph. Inf. Serv. 59, 142–143 (1983).
Andres, A.J. & Thummel, C.S. Methods for quantitative analysis of transcription in larvae and prepupae. Methods Cell Biol. 44, 565–573 (1994).
Diehl, F., Grahlmann, S., Beier, M. & Hoheisel, J.D. Manufacturing DNA microarrays of high spot homogeneity and reduced background signal. Nucleic Acids Res. 29, e38 (2001).
Yang, Y.H., Buckley, M.J., Dudoit, S. & Speed, T.P. Comparison of methods for image analysis on cDNA microarray data. J. Comput. Graph. Stat. 11, 108–136 (2002).
Yang, Y.H., Dudoit, S., Luu, P. & Speed, T.P. Normalization for cDNA microarray data. Proc. SPIE 4266, 141–152 (2001).
Kerr, M.K., Martin, M. & Churchill, G.A. Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819–837 (2000).
Martins, E.P. Estimating the rate of phenotypic evolution from comparative data. Am. Nat. 144, 193–209 (1994).
Hansen, T.F. & Martins, E.P. Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50, 1404–1417 (1996).
Sokal, R.R. & Rohlf, F.J. Biometry (W.H. Freeman and Company, New York, 1995).
Li, Y.J., Satta, Y. & Takahata, N. Paleo-demography of the Drosophila melanogaster subgroup: application of the maximum likelihood method. Genes Genet. Syst. 74, 117–127 (1999).
Swofford, D.L. PAUP*: phylogenetic analysis using parsimony (and other methods), edn 4.0 (Sinauer, Sunderland, MA, 1996).
Thummel, C.S. Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev. Cell 1, 453–465 (2001).
Acknowledgements
We thank A. Davis for the Netherlands2 line, and M. Feldman, B. Null, P. Lizardi, J. Leamon, P. Magwene, G. Wagner, S. Rice, J.D.Lambert, T.-R. Li, N. Carriero and members of the Kim and White laboratories for advice, support and technical help. This research was supported by the National Institutes of Health.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
Rifkin, S., Kim, J. & White, K. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet 33, 138–144 (2003). https://doi.org/10.1038/ng1086
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng1086
This article is cited by
-
Comparative single-cell transcriptomic analysis of primate brains highlights human-specific regulatory evolution
Nature Ecology & Evolution (2023)
-
Comparative transcriptomics between Drosophila mojavensis and D. arizonae reveals transgressive gene expression and underexpression of spermatogenesis-related genes in hybrid testes
Scientific Reports (2021)
-
Integrative phenotypic and gene expression data identify myostatin as a muscle growth inhibitor in Chinese shrimp Fenneropenaeus chinensis
Scientific Reports (2020)
-
Development of fly tolerance to consuming a high-protein diet requires physiological, metabolic and transcriptional changes
Biogerontology (2020)
-
Expression Divergence as an Evolutionary Alternative Mechanism Adopted by Two Rice Subspecies Against Rice Blast Infection
Rice (2019)