The Hourglass and the Early Conservation Models—Co-Existing Patterns of Developmental Constraints in Vertebrates

English version České info

Developmental constraints have been postulated to limit the space of feasible phenotypes and thus shape animal evolution. These constraints have been suggested to be the strongest during either early or mid-embryogenesis, which corresponds to the early conservation model or the hourglass model, respectively. Conflicting results have been reported, but in recent studies of animal transcriptomes the hourglass model has been favored. Studies usually report descriptive statistics calculated for all genes over all developmental time points. This introduces dependencies between the sets of compared genes and may lead to biased results. Here we overcome this problem using an alternative modular analysis. We used the Iterative Signature Algorithm to identify distinct modules of genes co-expressed specifically in consecutive stages of zebrafish development. We then performed a detailed comparison of several gene properties between modules, allowing for a less biased and more powerful analysis. Notably, our analysis corroborated the hourglass pattern at the regulatory level, with sequences of regulatory regions being most conserved for genes expressed in mid-development but not at the level of gene sequence, age, or expression, in contrast to some previous studies. The early conservation model was supported with gene duplication and birth that were the most rare for genes expressed in early development. Finally, for all gene properties, we observed the least conservation for genes expressed in late development or adult, consistent with both models. Overall, with the modular approach, we showed that different levels of molecular evolution follow different patterns of developmental constraints. Thus both models are valid, but with respect to different genomic features.

Vyšlo v časopise: The Hourglass and the Early Conservation Models—Co-Existing Patterns of Developmental Constraints in Vertebrates. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003476
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003476

Souhrn

Zdroje

1. PoeS, WakeMH (2004) Quantitative tests of general models for the evolution of development. Am Nat 164: 415–22.

2. von Baer KE (1828) Ueber Entwicklungsgeschichte der Thiere: Beobachtung und Reexion. Königsberg: Bornträger.

3. SeidelF (1960) Körpergrundgestalt und keimstruktur. eine erörterung über die grundlagen der vergleichenden und experimentellen embryologie und deren gültigkeit bei phylogenetischen überlegungen. Zool Anz 164: 245–305.

4. Sander K (1983) The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. In: Goodwin BC WC Holder N, editor, Development and evolution. Cambridge University Press, pp. 137–159.

5. Elinson R (1987) Change in developmental patterns: Embryos of amphibians with large eggs. In: Raff RA RE, editor, Development as an Evolutionary Process. New York: Alan R. Liss., pp. 1–21.

6. DubouleD (1994) Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate bauplan and the evolution of morphologies through heterochrony. Dev Suppl 135–42.

7. Raff RA (1996) The shape of life: genes, development, and the evolution of animal form. Chicago; London: University of Chicago Press.

8. Prud'hommeB, GompelN (2010) Evolutionary biology: Genomic hourglass. Nature 468: 768–9.

9. KalinkaA, TomancakP (2012) The evolution of early animal embryos: conservation or divergence? Trends in Ecology & Evolution 27: 385–393.

10. Hazkani-CovoE, WoolD, GraurD (2005) In search of the vertebrate phylotypic stage: a molecular examination of the developmental hourglass model and von Baer's third law. J Exp Zool B Mol Dev Evol 304: 150–8.

11. Domazet-LošoT, TautzD (2010) A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468: 815–8.

12. KalinkaAT, VargaKM, GerrardDT, PreibischS, CorcoranDL, et al. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811–4.

13. IrieN, KurataniS (2011) Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2: 248.

14. QuintM, DrostHG, GabelA, UllrichKK, BönnM, et al. (2012) A transcriptomic hourglass in plant embryogenesis. Nature

15. McDonald JH (2009) Handbook of Biological Statistics (2nd ed.). Baltimore, Maryland: Sparky House Publishing.

16. Speed T (2000) Always log spot intensities and ratios. Available: http://www.stat.berkeley.edu/users/terry/zarray/Html/log.html. Accessed 20 March 2013.

17. RouxJ, Robinson-RechaviM (2008) Developmental constraints on vertebrate genome evolution. PLoS Genet 4: e1000311 doi:10.1371/journal.pgen.1000311.

18. ComteA, RouxJ, Robinson-RechaviM (2010) Molecular signaling in zebrafish development and the vertebrate phylotypic period. Evolution & development 12: 144–156.

19. BergmannS, IhmelsJ, BarkaiN (2003) Iterative signature algorithm for the analysis of large-scale gene expression data. Phys Rev E Stat Nonlin Soft Matter Phys 67: 031902.

20. IhmelsJ, BergmannS, BarkaiN (2004) Defining transcription modules using large-scale gene expression data. Bioinformatics 20: 1993–2003.

21. AanesH, WinataCL, LinCH, ChenJP, SrinivasanKG, et al. (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 21: 1328–38.

22. KrumlaufR (1994) Hox genes in vertebrate development. Cell 78: 191–201.

23. HartleyRS, RempelRE, MallerJL (1996) In vivo regulation of the early embryonic cell cycle in Xenopus. Dev Biol 173: 408–19.

24. YardenA, GeigerB (1996) Zebrafish cyclin E regulation during early embryogenesis. Dev Dyn 206: 1–11.

25. IrieN, Sehara-FujisawaA (2007) The vertebrate phylotypic stage and an early bilaterian-related stage in mouse embryogenesis defined by genomic information. BMC Biol 5: 1.

26. Ohno S, et al.. (1970) Evolution by gene duplication. Berlin, Heidelberg and New York: Springer- Verlag.

27. ZhangJ (2003) Evolution by gene duplication - an update. Trends Ecol Evol 18: 292–298.

28. NeiM (2007) The new mutation theory of phenotypic evolution. Proc Natl Acad Sci U S A 104: 12235–42.

29. WangX, GrusWE, ZhangJ (2006) Gene losses during human origins. PLoS Biol 4: e52 doi:10.1371/journal.pbio.0040052.

30. DemuthJP, HahnMW (2009) The life and death of gene families. Bioessays 31: 29–39.

31. VilellaAJ, SeverinJ, Ureta-VidalA, HengL, DurbinR, et al. (2009) EnsemblCompara genetrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327–35.

32. KingMC, WilsonAC (1975) Evolution at two levels in humans and chimpanzees. Science 188: 107–16.

33. PreussTM, CáceresM, OldhamMC, GeschwindDH (2004) Human brain evolution: insights from microarrays. Nat Rev Genet 5: 850–60.

34. CarrollSB (2005) Evolution at two levels: on genes and form. PLoS Biol 3: e245 doi:10.1371/journal.pbio.0030245.

35. JordanIK, Mariño-RamírezL, WolfYI, KooninEV (2004) Conservation and coevolution in the scale-free human gene coexpression network. Mol Biol Evol 21: 2058–70.

36. YanaiI, GraurD, OphirR (2004) Incongruent expression profiles between human and mouse orthologous genes suggest widespread neutral evolution of transcription control. OMICS 8: 15–24.

37. JordanIK, Marino-RamirezL, KooninEV (2005) Evolutionary significance of gene expression divergence. Gene 345: 119–126.

38. WangQT, PiotrowskaK, CiemerychMA, MilenkovicL, ScottMP, et al. (2004) A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6: 133–44.

39. Bastian F, Parmentier G, Roux J, Moretti S, Laudet V, et al.. (2008) Bgee: Integrating and comparing heterogeneous transcriptome data among species. In: Bairoch A, Cohen-Boulakia S, Froidevaux C, editors, Data Integration in the Life Sciences, Springer Berlin/Heidelberg, volume 5109 of Lecture Notes in Computer Science. pp. 124–131.

40. SternDL (2000) Evolutionary developmental biology and the problem of variation. Evolution 54: 1079–91.

41. WrayGA (2007) The evolutionary signi_cance of cis-regulatory mutations. Nat Rev Genet 8: 206–16.

42. CarrollSB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25–36.

43. EngströmPG, FredmanD, LenhardB (2008) Ancora: a web resource for exploring highly conserved noncoding elements and their association with developmental regulatory genes. Genome Biol 9: R34.

44. SimonsC, MakuninIV, PheasantM, MattickJS (2007) Maintenance of transposon-free regions throughout vertebrate evolution. BMC Genomics 8: 470.

45. SandelinA, BaileyP, BruceS, EngströmPG, KlosJM, et al. (2004) Arrays of ultraconserved noncoding regions span the loci of key developmental genes in vertebrate genomes. BMC Genomics 5: 99.

46. WoolfeA, GoodsonM, GoodeDK, SnellP, McEwenGK, et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3: e7 doi:10.1371/journal.pbio.0030007.

47. VavouriT, WalterK, GilksWR, LehnerB, ElgarG (2007) Parallel evolution of conserved noncoding elements that target a common set of developmental regulatory genes from worms to humans. Genome Biol 8: R15.

48. IrimiaM, TenaJJ, AlexisM, Fernandez-MiñanA, MaesoI, et al. (2012) Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res

49. KimmelCB, BallardWW, KimmelSR, UllmannB, SchillingTF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253–310.

50. EdgarR, DomrachevM, LashAE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207–10.

51. HubbardTJP, AkenBL, AylingS, BallesterB, BealK, et al. (2009) Ensembl 2009. Nucleic Acids Res 37: D690–7.

52. SmedleyD, HaiderS, BallesterB, HollandR, LondonD, et al. (2009) BioMart – biological queries made easy. BMC Genomics 10: 22.

53. AlexaA, RahnenfuhrerJ, LengauerT (2006) Improved scoring of functional groups from gene expression data by decorrelating go graph structure. Bioinformatics 22: 1600–1607.

54. FlicekP, AhmedI, Amode MRS, BarrellD, BealK, et al. (2013) Ensembl 2013. Nucleic Acids Res 41: D48–55.

55. Gouveia-OliveiraR, SackettPW, PedersenAG (2007) MaxAlign: maximizing usable data in alignment. BMC Bioinformatics 8: 312.

56. YangZ (2007) PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol 24: 1586–91.

57. WolfYI, NovichkovPS, KarevGP, KooninEV, LipmanDJ (2009) The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proc Natl Acad Sci U S A 106: 7273–80.