Population genetics of cis-regulatory sequences that operate during embryonic development in the sea urchin Strongylocentrotus purpuratus

Evolution and Development

Volumn 14, Issue 2, 2012, Pages 152-167

  Garfield, David ^a,b   Haygood, Ralph ^a   Nielsen, William J ^a   Wray, Gregory A ^a  

^a DUKE UNIVERSITY   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ECHINODERM; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC VARIATION; MOLECULAR ANALYSIS; MUTATION; POPULATION GENETICS;

ANIMAL; ARTICLE; DEVELOPMENTAL GENE; GENE EXPRESSION REGULATION; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; GENETICS; MOLECULAR EVOLUTION; MUTATION; PRENATAL DEVELOPMENT; REGULATORY SEQUENCE; STRONGYLOCENTROTUS;

ANIMALS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DEVELOPMENTAL; GENETIC HETEROGENEITY; MUTATION; POLYMORPHISM, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; STRONGYLOCENTROTUS PURPURATUS;

ECHINOIDEA; STRONGYLOCENTROTUS PURPURATUS;

EID: 84864015643     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2012.00532.x     Document Type: Article

References (101)

1. Addison, J. A., and Hart, M. W. 2003. Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites. Mar. Biol. 144: 243-251.
2. Addison, J. A., and Hart, M. W. 2005. Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution 59: 532-543.
3. Balhoff, J. P., and Wray, G. A. 2005. Evolutionary analysis of the well characterized endo16 promoter reveals substantial variation within functional sites. Proc. Natl. Acad. Sci. USA 102: 8591-8596.
4. Bamshad, M. J., et al 2002. A strong signature of balancing selection in the 5' cis-regulatory region of CCR5. Proc. Natl. Acad. Sci. USA 99: 10539-10544.
5. Biermann, C. H., Kessing, B. D., and Palumbi, S. R. 2003. Phylogeny and development of marine model species: strongylocentrotid sea urchins. Evol. Dev. 5: 360-371.
6. Blanchette, M., et al 2006. Genome-wide computational prediction of transcriptional regulatory modules reveals new insights into human gene expression. Genome Res. 16: 656-668.
7. Blow, M. J., et al 2010. ChIP-Seq identification of weakly conserved heart enhancers. Nat. Genet. 42: 806-810.
8. Britten, R. J. 2010. Transposable element insertions have strongly affected human evolution. Proc. Natl. Acad. Sci. USA 107: 19945-19948.
9. Bullaughey, K. 2011. Changes in selective effects over time facilitate turnover of enhancer sequences. Genetics 187: 567-582.
10. Cameron, R. A., Britten, R. J., and Davidson, E. H. 1989. Expression of two actin genes during larval development in the sea urchin Strongylocentrotus purpuratus. Mol. Reprod. Dev. 1: 149-155.
11. Cameron, R. A., et al 2005. An evolutionary constraint: strongly disfavored class of change in DNA sequence during divergence of cis-regulatory modules. Proc. Natl. Acad. Sci. USA 102: 11769-11774.
12. Cameron, R. A., Samanta, M., Yuan, A., He, D., and Davidson, E. 2009. SpBase: the sea urchin genome database and web site. Nucleic Acids Res. 37: D750-D754.
13. Carroll, S. B. 2005. Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom. W.W. Norton & Co, New York.
14. Chan, Y. F., et al 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
15. Colosimo, P. F., et al 2005. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307: 1928-19233.
16. Cox, K. H., Angerer, L. M., Lee, J. J., Davidson, E. H., and Angerer, R. C. 1986. Cell lineage-specific programs of expression of multiple actin genes during sea urchin embryogenesis. J. Mol. Biol. 188: 159-172.
17. Davidson, E. H., McClay, D. R., and Hood, L. 2003. Regulatory gene networks and the properties of the developmental process. Proc. Natl. Acad. Sci. USA 100: 1475-1480.
18. Edmands, S., Moberg, P. E., and Burton, R. S. 1996. Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin. Mar. Biol. 126: 443-450.
19. Fay, J. C., and Benavides, J. A. 2005. Hypervariable noncoding sequences in Saccharomyces cerevisiae. Genetics 170: 1575-1587.
20. Fay, J. C., and Wu, C. I. 2000. Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
21. Flowers, J. M., Schroeter, S. C., and Burton, R. S. 2002. The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus. Evolution 56: 1445-1453.
22. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
23. Fu, Y. X., and Li, W. H. 1993. Statistical tests of neutrality of mutations. Genetics 133: 693-709.
24. Ge, B., et al 2009. Global patterns of cis- variation in human cells revealed by high-density allelic expression analysis. Nat. Genet. 41: 1216-1222.
25. Ghiglione, C., Emily-Fenouil, F., Lhomond, G., and Gache, C. 1997. Organization of the proximal promoter of the hatching-enzyme gene, the earliest zygotic gene expressed in the sea urchin embryo. Eur. J. Biochem. 250: 502-513.
26. Gilad, Y., Rifkin, S. A., and Pritchard, J. K. 2008. Revealing the architecture of gene regulation: the promise of eQTL studies. Trends Genet. 24: 408-415.
27. Gimelfarb, A. 1989. Genotypic variation for a quantitative character maintained under stabilizing selection without mutations: epistasis. Genetics 123: 217-227.
28. Greenberg, A. J., and Wu, C. I. 2006. Molecular genetics of natural populations. Mol. Biol. Evol. 23: 883-886.
29. Hamblin, M. T., and Di Rienzo, A. 2000. Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am. J. Hum. Genet. 66: 1669-1679.
30. Hancock, J. M., Shaw, P. J., Bonneton, F., and Dover, G. A. 1999. High sequence turnover in the regulatory regions of the developmental gene hunchback in insects. Mol. Biol. Evol. 16: 253-265.
31. He, B. Z., Holloway, A. K., Maerkl, S. J., and Kreitman, M. 2011. Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules. PLoS Genet. 7: e1002053.
32. He, Q., et al 2011. High conservation of transcription factor binding and evidence for combinatorial regulation across six Drosophila species. Nat. Genet. 43: 414-420.
33. Hein, J., Schierup, M. H., and Wiuf, C. 2005. Gene Genealogies, Variation and Evolution: A Primer in Coalescent Theory. Oxford University Press, Oxford; New York.
34. Hudson, R. R. 2001. Two-locus sampling distributions and their application. Genetics 159: 1805-1817.
35. Hudson, R. R. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338.
36. Hughes, J. R., et al 2005. Annotation of cis-regulatory elements by identification, subclassification, and functional assessment of multispecies conserved sequences. Proc. Natl. Acad. Sci. USA 102: 9830-9835.
37. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
38. Janes, D. E., et al 2011. Reptiles and mammals have differentially retained long conserved noncoding sequences from the amniote ancestor. Genome Biol. Evol. 3: 102-113.
39. Jenkins, D. L., Ortori, C. A., and Brookfield, J. F. 1995. A test for adaptive change in DNA sequences controlling transcription. Proc. Biol. Sci. 261: 203-207.
40. Jensen, J. D., Kim, Y., DuMont, V. B., Aquadro, C. F., and Bustamante, C. D. 2005. Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170: 1401-1410.
41. Kasowski, M., et al 2010. Variation in transcription factor binding among humans. Science 328: 232-235.
42. Keightley, P. D., Lercher, M. J., and Eyre-Walker, A. 2005. Evidence for widespread degradation of gene control regions in hominid genomes. PLoS Biol. 3: e42.
43. Kellis, M., Patterson, N., Endrizzi, M., Birren, B., and Lander, E. S. 2003. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241-254.
44. Kissinger, J. C., Hahn, J. H., and Raff, R. A. 1997. Rapid evolution in a conserved gene family. Evolution of the actin gene family in the sea urchin genus Heliocidaris and related genera. Mol. Biol. Evol. 14: 654-665.
45. Kissinger, J. C., and Raff, R. A. 1998. Evolutionary changes in sites and timing of actin gene expression in embryos of the direct- and indirect-developing sea urchins, Heliocidaris erythrogramma and H. tuberculata. Dev. Genes. Evol. 208: 82-93.
46. Knight, J. C. 2005. Regulatory polymorphisms underlying complex disease traits. J. Mol. Med. 83: 97-109.
47. Kozlowski, D. J., Gagnon, M. L., Marchant, J. K., Reynolds, S. D., Angerer, L. M., and Angerer, R. C. 1996. Characterization of a SpAN promoter sufficient to mediate correct spatial regulation along the animal-vegetal axis of the sea urchin embryo. Dev. Biol. 176: 95-107.
48. Lappalainen, T., and Dermitzakis, E. T. 2010. Evolutionary history of regulatory variation in human populations. Hum. Mol. Genet. 19: R197-R203.
49. Lee, J. J., Calzone, F. J., and Davidson, E. H. 1992. Modulation of sea urchin actin mRNA prevalence during embryogenesis: nuclear synthesis and decay rate measurements of transcripts from five different genes. Dev. Biol. 149: 415-431.
50. Lee, Y. H. 2003. Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida. Mol. Biol. Evol. 20: 1211-1221.
51. Lemos, B., Meiklejohn, C. D., Caceres, M., and Hartl, D. L. 2005. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 59: 126-137.
52. Lepage, T., and Gache, C. 1989. Purification and characterization of the sea urchin embryo hatching enzyme. J. Biol. Chem. 264: 4787-4793.
53. Lepage, T., Sardet, C., and Gache, C. 1992. Spatial expression of the hatching enzyme gene in the sea urchin embryo. Dev. Biol. 150: 23-32.
54. Littlewood, D. T. J., and Smith, A. B. 1995. A combined morphological and molecular phylogeny for sea urchins (Echinoidea, Echinodermata). Philos. Trans. R. Soc. Lond. B 347: 213-234.
55. Liu, X. Y., et al 2006. An ancient balanced polymorphism in a regulatory region of human major histocompatibility complex is retained in Chinese minorities but lost worldwide. Am. J. Hum. Genet. 78: 393-400.
56. Liu, Y., Liu, X. S., Wei, L., Altman, R. B., and Batzoglou, S. 2004. Eukaryotic regulatory element conservation analysis and identification using comparative genomics. Genome Res. 14: 451-458.
57. Ludwig, M. Z. 2002. Functional evolution of noncoding DNA. Curr. Opin. Genet. Dev. 12: 634-639.
58. Ludwig, M. Z., Bergman, C., Patel, N. H., and Kreitman, M. 2000. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403: 564-567.
59. Ludwig, M. Z., and Kreitman, M. 1995. Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol. Biol. Evol. 12: 1002-1011.
60. Lusk, R. W., and Eisen, M. B. 2010. Evolutionary mirages: Selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet. 6: e1000829.
61. Macdonald, S. J., and Long, A. D. 2005. Identifying signatures of selection at the enhancer of split neurogenic gene complex in Drosophila. Mol. Biol. Evol. 22: 1159-1159.
62. Maddison, W. P., and Maddison, D. R. 2010. Mesquite: a modular system for evolutionary analysis.
63. McClay, D. R. 2011. Evolutionary crossroads in developmental biology: sea urchins. Development 138: 2639-2648.
64. McDonald, J. H., and Kreitman, M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652-654.
65. McGregor, A. P., et al 2001. Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: implications for molecular coevolution. Evol. Dev. 3: 397-407.
66. McLean, C., and Bejerano, G. 2008. Dispensability of mammalian DNA. Genome Res. 18: 1743-1751.
67. Miller, B. A., and Emlet, R. B. 1997. Influence of nearshore hydrodynamics on larval abundance and settlement of sea urchins Strongylocentrotus franciscanus and S. purpuratus in the Oregon upwelling zone. Mar. Ecol. Prog. Ser. 148: 83-94.
68. Morgenstern, B. 1999. DIALIGN 2: improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics 15: 211-218.
69. Ohta, T. 2002. Near-neutrality in evolution of genes and gene regulation. Proc. Natl. Acad. Sci. USA 99: 16134-16137.
70. Oliveri, P., Tu, Q., and Davidson, E. H. 2008. Global regulatory logic for specification of an embryonic cell lineage. Proc. Natl. Acad. Sci. USA 105: 5955-5962.
71. Palumbi, S. R., and Wilson, A. C. 1990. Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and Strongylocentrotus-droebachiensis. Evolution 44: 403-415.
72. Peter, I. S., and Davidson, E. H. 2011. A gene regulatory network controlling the embryonic specification of endoderm. Nature 474: 635-639.
73. Phinchongsakuldit, J., MacArthur, S., and Brookfield, J. F. 2004. Evolution of developmental genes: molecular microevolution of enhancer sequences at the Ubx locus in Drosophila and its impact on developmental phenotypes. Mol. Biol. Evol. 21: 348-363.
74. Pollard, D. A., Moses, A. M., Iyer, V. N., and Eisen, M. B. 2006. Detecting the limits of regulatory element conservation and divergence estimation using pairwise and multiple alignments. BMC Bioinform. 7: 376.
75. Prabhakar, S., Noonan, J. P., Paabo, S., and Rubin, E. M. 2006. Accelerated evolution of conserved noncoding sequences in humans. Science 314: 786.
76. Przeworski, M. 2002. The signature of positive selection at randomly chosen loci. Genetics 160: 1179-89.
77. Rebeiz, M., Pool, J. E., Kassner, V. A., Aquadro, C. F., and Carroll, S. B. 2009. Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326: 1663-1667.
78. Rifkin, S. A., Houle, D., Kim, J., and White, K. P. 2005. A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression. Nature 438: 220-223.
79. Rifkin, S. A., Kim, J., and White, K. P. 2003. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat. Genet. 33: 138-144.
80. Rockman, M. V., Hahn, M. W., Soranzo, N., Goldstein, D. B., and Wray, G. A. 2003. Positive selection on a human-specific transcription factor binding site regulating IL4 expression. Curr. Biol. 13: 2118-2123.
81. Rockman, M. V., Hahn, M. W., Soranzo, N., Loisel, D. A., Goldstein, D. B., and Wray, G. A. 2004. Positive selection on MMP3 regulation has shaped heart disease risk. Curr. Biol. 14: 1531-1539.
82. Rockman, M. V., and Wray, G. A. 2002. Abundant raw material for cis-regulatory evolution in humans. Mol. Biol. Evol. 19: 1991-2004.
83. Romano, L. A., and Wray, G. A. 2003. Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation. Development 130: 4187-4199.
84. Shin, H. D., et al 2000. Genetic restriction of HIV-1 pathogenesis to AIDS by promoter alleles of IL10. Proc. Natl. Acad. Sci. USA 97: 14467-14472.
85. Siepel, A., et al 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15: 1034-1050.
86. Stark, A., et al 2007. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219-232.
87. Stranger, B. E., et al 2007. Population genomics of human gene expression. Nat. Genet. 39: 1217-1224.
88. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
89. Torgerson, D. G., et al 2009. Evolutionary processes acting on candidate cis-regulatory regions in humans inferred from patterns of polymorphism and divergence. PLoS Genet. 5: e1000592.
90. Tung, J., Primus, A., Bouley, A. J., Severson, T. F., Alberts, S. C., and Wray, G. A. 2009. Evolution of a malaria resistance gene in wild primates. Nature 460: 388-391.
91. Visel, A., et al 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 40: 158-160.
92. Walters, J., Binkley, E., Haygood, R., and Romano, L. A. 2008. Evolutionary analysis of the cis-regulatory region of the spicule matrix gene SM50 in strongylocentrotid sea urchins. Dev. Biol. 315: 567-578.
93. Wang, A. V., et al 1994. Distinct pattern of embryonic expression of the sea urchin CyI actin gene in Tripneustes gratilla. Dev. Biol. 165: 117-125.
94. Wardle, F. C., Angerer, L. M., Angerer, R. C., and Dale, L. 1999. Regulation of BMP signaling by the BMP1/TLD-related metalloprotease, SpAN. Dev. Biol. 206: 63-72.
95. Wayne, M. L., and Simonsen, K. L. 1998. Statistical tests of neutrality in the age of weak selection. Trends Ecol. Evol. 13: 236-240.
96. Wei, Z., Angerer, L. M., Gagnon, M. L., and Angerer, R. C. 1995. Characterization of the SpHE promoter that is spatially regulated along the animal-vegetal axis of the sea urchin embryo. Dev. Biol. 171: 195-211.
97. Wratten, N. S., McGregor, A. P., Shaw, P. J., and Dover, G. A. 2006. Evolutionary and functional analysis of the tailless enhancer in Musca domestica and Drosophila melanogaster. Evol. Dev. 8: 6-15.
98. Wray, G. A. 2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8: 206-216.
99. Wray, G. A., et al 2003. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20: 1377-1419.
100. Zhang, Z., and Gerstein, M. 2003. Of mice and men: phylogenetic footprinting aids the discovery of regulatory elements. J. Biol. 2: 11.
101. Zheng, W., Zhao, H., Mancera, E., Steinmetz, L. M., and Snyder, M. 2010. Genetic analysis of variation in transcription factor binding in yeast. Nature 464: 1187-1191.