Gene expression divergence recapitulates the developmental hourglass model

Nature

Volumn 468, Issue 7325, 2010, Pages 811-816

  Kalinka, Alex T ^a   Varga, Karolina M ^a,d   Gerrard, Dave T ^b   Preibisch, Stephan ^a   Corcoran, David L ^c   Jarrells, Julia ^a   Ohler, Uwe ^c   Bergman, Casey M ^b   Tomancak, Pavel ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c DUKE UNIVERSITY   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONSERVATION GENETICS; DIVERGENCE; EMBRYO; FLY; GENE EXPRESSION; MORPHOLOGY; NATURAL SELECTION; SPECIATION (BIOLOGY);

ARTHROPOD; ARTICLE; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE SEQUENCE; GENETIC VARIABILITY; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; GENOME, INSECT; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; SELECTION, GENETIC; SPECIES SPECIFICITY; TIME FACTORS;

ANIMALIA; ARTHROPODA;

EID: 78650120369     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09634     Document Type: Article

References (50)

1. Duboule, D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev. Suppl.135-142 (1994).
2. Raff, R. A. The Shape of Life: Genes, Development and the Evolution of Animal Form (Univ Chicago Press, 1996).
3. Hall, B. K. Phylotypic stage or phantom, is there a highly conserved embryonic stage in vertebrates? Trends Ecol. Evol. 12, 461-463 (1997).
4. Sander, K. Specification of the basic body planininsect embryogenesis. Adv. Insect Physiol. 12, 125-238 (1976).
5. Wray, G. A. & Raff, R. A. Rapid evolution ofgastrulation mechanisms ina sea urchin with lecithotrophic larvae. Evolution 45, 1741-1750 (1991).
6. Goldstein, B., Frisse, L. M. & Thomas, W. K. Embryonic axis specification in nematodes: evolution of the first step in development. Curr. Biol. 8, 157-160 (1998).
7. Schmidt, K. & Starck, J. M. Developmental variability during early embryonic development of zebra fish, Danio rerio. J. Exp. Zoolog. B 302, 446-457 (2004).
8. Carroll, S. B. Evolution at two levels: on genes and form. PLoS Biol. 3, e245 (2005).
9. Wray, G. A. The evolutionary significance of cis-regulatory mutations. Nature Rev. Genet. 8, 206-216 (2007).
10. Von Baer, K. E. Uber Entwickelungsgeschichte der Thiere: Beobachtung und Reflektion (Königsberg, 1828).
11. Darwin, C. On the Origin of Species (Murray, 1859).
12. Garstang, W. The theory of recapitulation: a critical restatement of the biogenetic law. Linn. J. Zool 35, 81-101 (1922).
13. Sander, K. The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. In Development and Evolution 137-159C (Cambridge Univ. Press, 1983).
14. Galis, F. & Metz, J. A. Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservation. J. Exp. Zool. 291, 195-204 (2001).
15. Hazkani-Covo, E., Wool, D. & Graur, D. In search of the vertebrate phylotypic stage: a molecular examination of the developmental hourglass model and von Baer's third law. J. Exp. Zoolog. B 304, 150-158 (2005).
16. Davis, J. C., Brandman, O. & Petrov, D. A. Protein evolution in the context of Drosophila development. J. Mol. Evol. 60, 774-785 (2005).
17. Cruickshank, T. & Wade, M. J. Microevolutionary support for a developmental hourglass: gene expression patterns shape sequence variation and divergence in Drosophila. Evol. Dev. 10, 583-590 (2008).
18. Richardson, M. K. et al. There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat. Embryol. (Berl.) 196, 91-106 (1997).
19. Bininda-Emonds, O. R. P., Jeffery, J. E. & Richardson, M. K. Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development. Proc. R. Soc. Lond. B 270, 341-346 (2003).
20. Poe, S. & Wake, M. H. Quantitative tests of general models for the evolution of development. Am. Nat. 164, 415-422 (2004).
21. Tomancak, P. et al. Global analysis of patterns ofgene expression during Drosophila embryogenesis. Genome Biol. 8, R145 (2007).
22. Zhang, Y., Sturgill, D., Parisi, M., Kumar, S. & Oliver, B. Constraint and turnover in sex-biasedgene expression in the genus Drosophila. Nature 450, 233-237 (2007).
23. Bedford, T. & Hartl, D. L. Optimization of gene expression by natural selection. Proc. Natl Acad. Sci. USA 106, 1133-1138 (2009).
24. Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717-745 (2003).
25. Butler, M. A. & King, A. A. Phylogenetic comparative analysis: amodeling approach for adaptive evolution. Am. Nat. 164, 683-695 (2004).
26. Lemos, B., Meiklejohn, C. D., Cceres, M. & Hartl, D. L. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 59, 126-137 (2005).
27. Nelson, C. E., Hersh, B. M. & Carroll, S. B. The regulatory content of intergenic DNA shapes genome architecture. Genome Biol. 5, R25 (2004).
28. Nuzhdin, S. V., Wayne, M. L., Harmon, K. L. & McIntyre, L. M. Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol. Biol. Evol. 21, 1308-1317 (2004).
29. Artieri, C. G. & Singh, R. S. Molecular evidence for increased regulatory conservation during metamorphosis, and against deleterious cascading effects of hybrid breakdown in Drosophila. BMC Biol. 8, 26 (2010).
30. Rifkin, S. A., Kim, J. & White, K. P. Evolution of gene expression in the Drosophila melanogaster subgroup. Nature Genet. 33, 138-144 (2003).
31. Markow, T. A. & O'Grady, P. M. Drosophila biology inthe genomicage. Genetics 177, 1269-1276 (2007).
32. Ahmed, N., Natarajan,T. & Rao,K. R. Discrete cosine transform. IEEE Trans. Comput. C-23, 90-93 (1974).
33. Kerr, M. K., Martin, M. & Churchill, G. A. Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819-837 (2000).
34. Smyth, G. K. Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor 397-420 (Springer, 2005).
35. Smyth, G. K. Linear modelsand empirical Bayesmethods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
36. Irizarry, R. A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003).
37. Jonnalagadda, S. & Srinivasan, R. Principal components analysis based methodology to identify differentially expressed genes in time-course microarray data. BMC Bioinformatics 9, 267 (2008).
38. Felsenstein, J. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5, 164-166 (1989).
39. Huson, D. H. et al. Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8, 460 (2007).
40. Heger, A. & Ponting,C.P.Evolutionary rate analysesoforthologs and paralogs from 12 Drosophila genomes. Genome Res. 17, 1837-1849 (2007).
41. Paradis, E., Claude,J. & Strimmer, K. APE: Analyses ofPhylogenetics and Evolution in R language. Bioinformatics 20, 289-290 (2004).
42. Hansen, T. F. & Martins, E. P. Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50, 1404-1417 (1996).
43. Suzuki, R. & Shimodaira, H.Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540-1542 (2006).
44. Ge, Y., Dudoit, S. & Speed, T. P. Resampling-Based Multiple Testing for Microarray Data Analysis. Technical Report (Univ. California, 2003).
45. Alexa, A., Rahnenfhrer, J. & Lengauer, T. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22, 1600-1607 (2006).
46. Grossmann, S., Bauer, S., Robinson, P. N. & Vingron, M. Improved detection of overrepresentation of Gene-Ontology annotations with parent child analysis. Bioinformatics 23, 3024-3031 (2007).
47. Agudelo-Romero, P. et al. Changes in the gene expression profile of Arabidopsis thaliana after infection with Tobacco etch virus. Virol. J. 5, 92 (2008).
48. Larracuente, A. M. et al. Evolution of protein-coding genes in Drosophila. Trends Genet. 24, 114-123 (2008).
49. Smith, C. D., Shu, S., Mungall, C. J. & Karpen, G. H. The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316, 1586-1591 (2007).
50. Chintapalli, V. R., Wang, J. & Dow, J. A. T. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nature Genet. 39, 715-720 (2007).