The Relationship between Gene Network Structure and Expression Variation among Individuals and Species

English version České info

The variation generating mechanisms of development interact with the variation sorting mechanism of natural selection to produce organismal diversity. While the impacts of natural selection on existing variation have received much study, those of development on the generation of this variation remain less understood. This fundamental gap in our knowledge restricts our understanding of the key processes shaping evolution. In this study, we combine mathematical modeling, and population-level and cross-species assays of gene expression to investigate the relationship between the structure of the gene interactions regulating limb development and variation in the expression of limb genes among individuals and species. Results suggest that the way in which genes interact (i.e., development) biases the distribution of variation in gene expression among individuals, and that this in turn biases the distribution of variation among species.

Vyšlo v časopise: The Relationship between Gene Network Structure and Expression Variation among Individuals and Species. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005398
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005398

Souhrn

Zdroje

1. Draghi J, Parsons T, Wagner G, Plotkin J (2010) Mutational robustness can facilitate adaptation. Nature 463: 353–355. doi: 10.1038/nature08694 20090752

2. Parsons KJ, Marquez E, Albertson RC (2012) Constraint and opportunity: the genetic basis and evolution of modularity in the cichlid mandible. Am Nat 179: 64–78. doi: 10.1086/663200 22173461

3. Wagner GP (1988) The influence of variation and developmental constraints on the rate of multivariate phenotypic evolution. J Evol Biol 1: 45–66.

4. Darwin CR (1869) Origin of the species by means of natural selection, or the preservation of favoured races in the struggle for life. London, England: John Murray. 282 p.

5. Goldschmidt RB (1940) The material basis of evolution. New Haven, CT: Yale University Press. 436 p.

6. Waddington CH (1942) Canalization of development and the inheritance of acquired characteristics. Nature 150: 563–565.

7. Pigliucci M (2009) An extended synthesis for evolutionary biology. Ann N Y Acad Sci 1168: 218–228. doi: 10.1111/j.1749-6632.2009.04578.x 19566710

8. Polly PD (2007) Limbs in mammalian evolution. In: Hall BK, editor. Fins into Limbs: Evolution, Development, and Transformation. Chicago: University of Chicago Press. pp. 245–268.

9. Sheth R, Gregoire D, Dumouchel A, Scotti M, Pham J, et al. (2013) Decoupling the function of Hox and Shh in developing limb reveals multiple inputs of Hox genes on limb growth. Development 140: 2130–2138. doi: 10.1242/dev.089409 23633510

10. Rabinowitz AH, Vokes SA (2012) Integration of the transcriptional networks regulating limb morphogenesis. Dev Biol 368: 165–180. doi: 10.1016/j.ydbio.2012.05.035 22683377

11. Butterfield NC, McGlinn E, Wicking C (2010) The molecular regulation of vertebrate limb patterning. Curr Top Dev Biol 90: 319–341. doi: 10.1016/S0070-2153(10)90009-4 20691854

12. Zeller R, Lopez-Rios J, Zuniga A (2009) Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10: 845–858. doi: 10.1038/nrg2681 19920852

13. Bénazet JD, Bischofberger M, Tiecke E, Goncalves A, Martin JF, et al. (2009) A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323: 1050–1053. doi: 10.1126/science.1168755 19229034

14. Lewandoski M, Sun X, Martin GR (2000) Fgf8 signalling from the AER is essential for normal limb development. Nat Genet 26: 460–463. 11101846

15. Moon AM, Capecchi MR (2000) Fgf8 is required for outgrowth and patterning of the limbs. Nat Genet 26: 455–459. 11101845

16. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, et al. (1999) Fgf10 is essential for limb and lung formation. Nat Genet 21: 138–141. 9916808

17. Sun X, Mariani FV, Martin GR (2002) Functions of Fgf signalling from the apical ectodermal ridge in limb development. Nature 418: 501–508. 12152071

18. Pajni-Underwood S, Wilson CP, Elder C, Mishina Y, Lewandoski M (2007) Bmp signals control limb bud interdigital programmed cell death by regulating Fgf signaling. Development 134: 2359–2368. 17537800

19. Cooper KL, Hu JK, ten Berge D, Fernandez-Teran M, Ros MA, et al. (2011) Initiation of proximal-distal patterning in the vertebrate limb by signals and growth. Science 332: 1083–1086. doi: 10.1126/science.1199499 21617075

20. Barna M, Pandolfi PP, Niswander L (2005) Gli3 and Plzf cooperate in proximal limb patterning at early stages of limb development. Nature 436: 277–281. 16015334

21. Garfield DA, Runcie DE, Babbitt CC, Haygood R, Nielsen WJ, et al. (2013) The impact of gene expression variation on the robustness and evolvability of a developmental gene regulatory network. PLoS Biol 11: 1–16.

22. Galis F, Jacques JMvA, Metz JAJ (2001) Why five fingers? Evolutionary constraints on digit numbers. Trends Ecol Evol 16: 637–646.

23. Davidson EH, Erwin DH (2006) Gene regulatory networks and the evolution of animal body plans. Science 311: 796–800. 16469913

24. von Baer KE (1828) Entwicklungsgeschichte der Thiere: Beobachtung und Reflexion. Konigsberg: Borntrager. 264 p.

25. Raff RA (1996) The shape of life: genes, development, and the evolution of animal form. Chicago: University of Chicago Press. 544 p.

26. Carroll SB (2005) Evolution at two levels: On genes and form. PLoS Biol 3: 1159–1166.

27. Kalinka AT, Tomancak P (2012) The evolution of early animal embryos: conservation or divergence? Trends Ecol Evol 27: 385–393. doi: 10.1016/j.tree.2012.03.007 22520868

28. Duboule D, Wilkins AS (1998) The evolution of 'bricolage'. Trends Genet 14: 54–59. 9520598

29. Hinman VF, Nguyen AT, Cameron RA, Davidson EH (2003) Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci U S A 100: 13356–13361. 14595011

30. Lemons D, McGinnis W (2006) Genomic evolution of Hox gene clusters. Science 313: 1918–1922. 17008523

31. Garstang W (1922) The theory of recapitulation: a critical restatement of the Biogenetic law. J Exp Zool 291: 195–204.

32. de Beer GR (1954) Embryos and Ancestors, Revised edition. Oxford: Oxford University Press. 136 p.

33. Reidl R (1978) Order in living organisms: A systems analysis of evolution. New York, New York: Wiley. 313p.

34. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150: 563–565.

35. Ciliberti S, Martin OC, Wagner A (2007) Innovation and robustness in complex regulatory gene networks. Proc Natl Acad Sci U S A 104: 13591–13596. 17690244

36. Gursky VV, Surkova SY, Samsonova MG (2012) Mechanisms of developmental robustness. Biosystems 109: 329–335. doi: 10.1016/j.biosystems.2012.05.013 22687821

37. Wagner A (2011) Genotype networks shed light on evolutionary constraints. Trends Ecol Evol 26: 577–584. doi: 10.1016/j.tree.2011.07.001 21840080

38. He J, Deem MW (2010) Hierarchical evolution of animal body plans. Dev Biol 337: 157–161. doi: 10.1016/j.ydbio.2009.09.038 19799894

39. Erwin DH, Davidson EH (2009) The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10: 141–148. doi: 10.1038/nrg2499 19139764

40. Peter IS, Davidson EH (2011) Evolution of gene regulatory networks controlling body plan development. Cell 144: 970–985. doi: 10.1016/j.cell.2011.02.017 21414487

41. Artieri CG, Haerty W, Singh RS (2009) Ontogeny and phylogeny: molecular signatures of selection, constraint, and temporal pleiotropy in the development of Drosophila. BMC Biol 7: 42. doi: 10.1186/1741-7007-7-42 19622136

42. Roux J, Robinson-Rechavi M (2008) Developmental constraints on vertebrate genome evolution. PLoS Genet 4: e1000311. doi: 10.1371/journal.pgen.1000311 19096706

43. Davidson EH (2010) Emerging properties of animal gene regulatory networks. Nature 468: 911–920. doi: 10.1038/nature09645 21164479

44. Landry CR, Castillo-Davis CI, Ogura A, Liu JS, Hartl DL (2007) Systems-level analysis and evolution of the phototransduction network in Drosophila. Proc Natl Acad Sci U S A 104: 3283–3288. 17360639

45. Cooper K, Sears KE, Uygur A, Maier J, Stephan-Backowski K, et al. (2014) Patterning and post-patterning modes of evolutionary digit loss in mammals. Nature 511: 41–45. doi: 10.1038/nature13496 24990742

46. Hockman D, Cretekos CJ, Mason MK, Behringer RR, Jacobs DS, et al. (2008) A second wave of sonic hedgehog expression during the development of the bat limb. Proc Natl Acad Sci U S A 105: 16982–16987. doi: 10.1073/pnas.0805308105 18957550

47. Thewissen JGM, Cohn MJ, Stevens ME, Bajpai S, Heyning J, et al. (2006) Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proc Natl Acad Sci U S A 103: 8414–8418. 16717186

48. Keyte AL, Smith KK (2010) Developmental origins of precocial forelimbs in marsupial neonates Development 137: 4283–4294. doi: 10.1242/dev.049445 21098569

49. Sears KE, Doroba CK, Xie D, Zhong S (2012) Molecular determinants of marsupial limb integration and constraint. In: Müller J, Asher R, editors. From Clone to Bone: The Synergy of Morphological and Molecular Tools in Paleobiology. Cambridge: Cambridge University Press. pp. 257–278.

50. Cretekos CJ, Deng JM, Green ED, Rasweiler JJ, Behringer RR (2007) Isolation, genomic structure and developmental expression of Fgf8 in the short-tailed fruit bat, Carollia perspicillata. Int J Dev Biol 51: 333–338. 17554686

51. Chen CH, Cretekos CJ, Rasweiler JJ, Behringer RR (2005) Hoxd13 expression in the developing limbs of the short-tailed fruit bat, Carollia perspicillata. Evolution and Development 7: 130–141. 15733311

52. Ray R, Capecchi MR (2008) An examination of the chiropteran HoxD locus from an evolutionary perspective. Evolution and Development 10: 657–670. doi: 10.1111/j.1525-142X.2008.00279.x 19021736

53. Chew KY, Yu H, Pask AJ, Shaw G, Renfree MB (2012) Hoxa13 and Hoxd13 expression during development of the syndactylous digits in the marsupial Macropus eugenii. BMC Dev Biol 12: 2. doi: 10.1186/1471-213X-12-2 22235805

54. Gibson G, Dworkin I (2004) Uncovering cryptic genetic variation. Nat Rev Genet 5: 681–690. 15372091

55. Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, et al. (2013) Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342: 1372–1375. doi: 10.1126/science.1240276 24337296

56. Zeller R (2010) The temporal dynamics of vertebrate limb development, teratogenesis and evolution. Curr Opin Genet Dev 20: 384–390. doi: 10.1016/j.gde.2010.04.014 20537528

57. Sears KE, Patel A, Hübler M, Cao X, VandeBerg JL, et al. (2012) Disparate Igf1 expression and growth in the fore- and hind limbs of a marsupial (Monodelphis domestica). Exp Zool Part B 318: 279–293.

58. Cohn MJ, Tickle C (1999) Developmental basis of limblessness and axial patterning in snakes. Nature 399: 474–479. 10365960

59. Shubin N, Tabin C, Carroll S (1997) Fossils, genes and the evolution of animal limbs. Nature 388: 639–648. 9262397

60. Wanek N, Muneoka K, Holler-Dinsmore G, Burton R, Bryant SV (1989) A staging system for mouse limb development. J Exp Zool 249: 41–49. 2926360

61. Sokal RR, Rohlf FJ (1995) Biometry. New York: W.H. Freeman and Company. 880 p.

62. Cretekos CJ, Weatherbee SD, Chen CH, Badwaik NK, Niswander L, et al. (2005) Embryonic staging system for the short-tailed fruit bat, Carollia perspicillata, a model organism for the mammalian order Chiroptera, based upon timed pregnancies in captive-bred animals. Dev Dyn 233: 721–738. 15861401

63. Mate KE, Robinson ES, VandeBerg JL, Pederson RA (1994) Timetable of in vivo embryonic development in the gray short-tailed opossum (Monodelphis domestica). Mol Reprod Dev 39: 365–374. 7893485

64. McCrady E (1938) The embryology of the Opossum. Philadelphia: Wistar Institute of Anatomy and Biology. 233 p.

65. Butler H, Juurlink BHJ (1987) An Atlas for Staging Mammalian and Chick Embryos. Boca Raton, Florida: CRC Press. 218 p.