Parallel evolution of segmentation by co-option of ancestral gene regulatory networks

BioEssays

Volumn 32, Issue 1, 2010, Pages 60-70

  Chipman, Ariel D ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Body plans; Evolution; Fossil record; Gene regulatory networks; Segmentation

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL; ANTERIOR POSTERIOR AXIS; COMPARATIVE ANATOMY; EVOLUTIONARY ADAPTATION; GENE REGULATORY NETWORK; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PALEONTOLOGY; PHYLOGENY; PHYLUM; REVIEW;

ANIMALS; ANNELIDA; ARTHROPODS; BODY PATTERNING; CHORDATA; EVOLUTION; FOSSILS; GENE REGULATORY NETWORKS; HUMANS; MODELS, GENETIC; PHYLOGENY;

ANIMALIA;

EID: 74949090490     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.200900130     Document Type: Review

References (100)

1. Scholtz G. 2002. The Articulata hypothesis - or what is a segment? Org Divers Evol 2: 197-215.
2. Budd GE. 2001. Why are arthropods segmented? Evol Dev 3: 332-42.
3. Couso JP. 2009. Segmentation, metamerism and the Cambrian explosion. Int J Dev Biol 53: 1305-16.
4. Minelli A, Fusco G. 2004. Evo-devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19: 423-9.
5. Adoutte A, Balavoine G, Lartillot N, et al. 2000. The new animal phylogeny: reliability and implications. Proc Natl Acad Sci U S A 97: 4453-6.
6. Kimmel CB. 1996. Was Urbilateria segmented? Trends Genet 12: 329-31.
7. De Robertis EM. 2008. Evo-Devo: variations on ancestral themes. Cell 132: 185-95.
8. de Rosa R, Prud'homme B, Balavoine G. 2005. caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol Dev 7: 574-87.
9. Seaver EC. 2003. Segmentation: mono- or polyphyletic? Int J Dev Biol 47: 583-95.
10. Dequéant ML, Pourquié O. 2008. Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet 9: 370-82.
11. Lawrence PA. 1992. The Making of a Fly: The Genetics of Animal Design. Oxford, UK: Blackwell Scientific Publications.
12. Palmeirim I, Henrique D, Ish-Horowicz D, et al. 1997. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91: 639-48.
13. Jouve C, Palmeirim I, Henrique D, et al. 2000. Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127: 1421-9.
14. Aulehla A, Wehrle C, Brand-Saberi B, et al. 2003. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 4: 395-406.
15. Dubrulle J, Pourquié O. 2004. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427: 419-22.
16. Kawamura A, Koshida S, Hijikata H, et al. 2005. Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. Genes Dev 19: 1156-61.
17. Pourquié O. 2003. The segmentation clock: converting embryonic time into spatial pattern. Science 301: 328-30.
18. Rida PC, Le Minh N, Jiang YJ. 2004. A Notch feeling of somite segmentation and beyond. Dev Biol 265: 2-22.
19. Peel AD, Chipman AD, Akam M. 2005. Arthropod segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6: 905-16.
20. Stollewerk A, Schoppmeier M, Damen WGM. 2003. Involvement of Notch and Delta genes in spider segmentation. Nature 423: 863-5.
21. Chipman AD, Akam M. 2008. The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pairrule gene homologues. Dev Biol 319: 160-9.
22. Pueyo JI, Lanfear R, Couso JP. 2008. Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana. Proc Natl Acad Sci U S A 105: 16614-9.
23. Chipman AD, Arthur W, Akam M. 2004. A double segment periodicity underlies segment generation in centipede development. Curr Biol 14: 1250-5.
24. Schoppmeier M, Damen WGM. 2005. Expression of Pax group III genes suggests a single-segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei. Evol Dev 7: 160-9.
25. Irvine SM, Martindale MQ. 1996. Cellular and molecular mechanisms of segmentation in annelids. Sem Cell Dev Biol 7: 593-604.
26. Seaver EC, Shankland M. 2001. Establishment of segment polarity in the ectoderm of the leech Helobdella. Development 128: 1629-41.
27. Prud'homme B, de Rosa R, Arendt D, et al. 2003. Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Curr Biol 13: 1876-81.
28. Seaver EC, Kaneshige LM. 2006. Expression of 'segmentation' genes during larval and juvenile development in the polychaetes Capitella sp I and H. elegans. Dev Biol 289: 179-94.
29. Seaver EC, Thamm K, Hill SD. 2005. Growth patterns during segmentation in the two polychaete annelids, Capitella sp I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev 7: 312-26.
30. Rivera AS, Weisblat DA. 2009. And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Dev Genes Evol 219: 37-43.
31. Thamm K, Seaver EC. 2008. Notch signaling during larval and juvenile development in the polychaete annelid Capitella sp I. Dev Biol 320: 304-18.
32. Holland LZ, Kene M, Williams NA, et al. 1997. Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): The metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development 124: 1723-32.
33. Patel NH, Martin-Blanco E, Coleman KG, et al. 1989. Expression of engrailed protein in arthropods, annelids and chordates. Cell 58: 955-68.
34. Lans D, Wedeen CJ, Weisblat DA. 1993. Cell lineage analysis of the expression of an engrailed homolog in leech embryos. Development 117: 857-71.
35. Wedeen CJ, Weisblat DA. 1991. Segmental expression of an engrailedclass gene during early development and neurogenesis in an annelid. Development 113: 805-14.
36. Dunn CW, Hejnol A, Matus DQ, et al. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-50.
37. Telford MJ, Bourlat SJ, Economou A, et al. 2008. The evolution of the Ecdysozoa. Philos Trans R Soc Lond, B, Biol Sci 363: 1529-37.
38. Nielsen C. 2003. Proposing a solution to the Articulata-Ecdysozoa controversy. Zool Scr 32: 475-82.
39. Porter ML, Crandall KA. 2003. Lost along the way: the significance of evolution in reverse. Trends Ecol Evol 18: 541-7.
40. Jenner RA. 2004. When molecules and morphology clash: reconciling conflicting phylogenies of the Metazoa by considering secondary character loss. Evol Dev 6: 372-8.
41. Chipman AD. 2008. Annelids step forward. Evol Dev 10: 141-2.
42. Bleidorn C. 2007. The role of character loss in phylogenetic reconstruction as exemplified for the Annelida. J Zool Syst Evol Res 45: 299-307.
43. Struck TH, Schult N, Kusen T, et al. 2007. Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 7: 57.
44. Hessling R, Westheide W. 2002. Are Echiura derived from a segmented ancestor? Immunohistochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol 252: 100-13.
45. Kristof A, Wollesen T, Wanninger A. 2008. Segmental mode of neural patterning in Sipuncula. Curr Biol 18: 1129-32.
46. Budd GE. 1999. The morphology and phylogenetic significance of Kerygmachela kierkegaardi Budd (Buen Formation, Lower Cambrian, N Greenland). Trans R Soc Edinb 89: 249-90.
47. Scholtz G. 1992. Cell lineage studies in the crayfish Cherax destructor (Crustacea. Decapoda): germ band formation, segmentation, and early neurogenesis. Rouxs Arch Dev Biol 202: 36.
48. Chipman AD. 2008. Thoughts and speculations on the ancestral arthropod segmentation pathway. In: Minelli A, Fusco G, eds. Evolving Pathways: Key Themes in Evolutionary Developmental Biology. Cambridge: Cambridge University Press. pp. 339-55.
49. Shu DG, Conway Morris S, Zhang ZF, et al. 2003. A new species of yunnanozoan with implications for deuterostome evolution. Science 299: 1380-4.
50. Chen JY, Huang DY, Li CW. 1999. An early Cambrian craniate-like chordate. Nature 402: 518-22.
51. Shu DG, Conway Morris S, Han J, et al. 2004. Ancestral echinoderms from the Chengjiang deposits of China. Nature 430: 422-8.
52. Gehling JG. 1987. Earliest known echinoderm - a new Ediacaran fossil from the Pound Subgroup of South Australia. Alcheringa 11: 337-45.
53. Jefferies RPS. 1978. The Ancestry of the Vertebrates. London: British Museum (Natural History).
54. Ruta M. 1999. Brief review of the stylophoran debate. Evol Dev 1: 123-35.
55. Smith AB. 2008. Deuterostomes in a twist: the origins of a radical new body plan. Evol Dev 10: 493-503.
56. Bourlat SJ, Juliusdottir T, Lowe CJ, et al. 2006. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444: 85-8.
57. Shu DG, Conway Morris S, Han J, et al. 2001. Primitive deuterostomes from the Chengjiang Lagerstatte (Lower Cambrian, China). Nature 414: 419-24.
58. Gee H. 2001. Palaeontology - on being vetulicolian. Nature 414: 407.
59. Aldridge RJ, Hou XG, Siveter DJ, et al. 2007. The systematics and phylogenetic relationships of vetulicolians. Palaeontology 50: 131-68.
60. Lacalli TC. 2002. Vetulicolians - are they deuterostomes? chordates? Bioessays 24: 208-11.
61. Donoghue PCJ, Purnell MA. 2009. Distinguishing heat from light in debate over controversial fossils. Bioessays 31: 178-89.
62. Eriksson BJ, Tait NN, Budd GE, et al. 2009. The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid. 1996). Dev Genes Evol. 219: 249-64.
63. Mayer G, Whitington PM. 2009. Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda. Dev Biol 335: 263-75.
64. Dong XP, Donoghue PCJ, Cunningham JA, et al. 2005. The anatomy, affinity, and phylogenetic significance of Markuelia. Evol Dev 7: 468-82.
65. Budd GE. 2001. Tardigrades as 'stem-group arthropods': the evidence from the Cambrian fauna. Zool Anz 240: 265-79.
66. Fedonkin MA, Waggoner BM. 1997. The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature 388: 868-71.
67. Conway Morris S, Caron JB. 2007. Halwaxiids and the early evolution of the lophotrochozoans. Science 315: 1255-8.
68. Conway Morris S, Peel JS. 1995. Articulated halkierids from the Lower Cambrian of north Greenland and their role in early protostome evolution. Philos Trans R Soc Lond, B, Biol Sci 347: 305-58.
69. Butterfield NJ. 2006. Hooking some stem-group "worms": fossil iophotrochozoans in the Burgess Shale. Bioessays 28: 1161-6.
70. Giribet G, Okusu A, Lindgren AR, et al. 2006. Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons. Proc Natl Acad Sci U S A 103: 7723-8.
71. Baguña J, Riutort M. 2004. The dawn of bilaterian animals: the case of acoelomorph flatworms. Bioessays 26: 1046-57.
72. Hejnol A, Martindale MQ. 2008. Acoel development supports a simple planula-like urbilaterian. Philos Trans R Soc Lond, B, Biol Sci 363: 1493-501.
73. Jacobs DK, Hughes NC, Fitz-Gibbon ST, et al. 2005. Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form. Evol Dev 7: 498-514.
74. Curtis D, Apfeld J, Lehmann R. 1995. nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development 121: 1899-910.
75. Torras R, Gonzalez-Crespo S. 2005. Posterior expression of nanos orthologs during embryonic and larval development of the anthozoan Nematostella vectensis. Int J Dev Biol 49: 895-9.
76. Torras R, Yanze N, Schmid V, et al. 2004. nanos expression at the embryonic posterior pole and the medusa phase in the hydrozoan Podocoryne carnea. Evol Dev 6: 362-71.
77. Lall S, Ludwig MZ, Patel NH. 2003. Nanos plays a conserved role in axial patterning outside of the diptera. Curr Biol 13: 224-9.
78. Copf T, Schroder R, Averof M. 2004. Ancestral role of caudal genes in axis elongation and segmentation. Proc Natl Acad Sci U S A 101: 17711-5.
79. Epstein M, Pillemer G, Yelin R, et al. 1997. Patterning of the embryo along the anterior-posterior axis: the role of the caudal genes. Development 124: 3805-14.
80. Hejnol A, Martindale MQ. 2008. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456: 382-U45.
81. Holland LZ, Holland ND. 1998. Developmental gene expression in Amphioxus: new insights into the evolutionary origin of vertebrate brain regions, neural crest and rostrocaudal segmentation. Am Zool 38: 647-58.
82. Shimizu T, Bae YK, Muraoka O, et al. 2005. Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev Biol 279: 125-41.
83. Shinmyo Y, Mito T, Matsushita T, et al. 2005. caudal is required for gnathal and thoracic patterning and for posterior elongation in the intermediate-germband cricket Gryllus bimaculatus. Mech Dev 122: 231-9.
84. Copf T, Rabet N, Celniker SE, et al. 2003. Posterior patterning genes and the identification of a unique body region in the brine shrimp Artemia franciscana. Development 130: 5915-27.
85. Liu PZ, Kaufman TC. 2005. even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect. Development 132: 2081-92.
86. Mito T, Kobayashi C, Sarashina I, et al. 2007. even-skipped has gaplike, pair-rule-like, and segmental functions in the cricket Gryllus bimaculatus, a basal, intermediate germ insect (Orthoptera). Dev Biol 303: 202-13.
87. Martin BL, Kimelman D. 2009. Wnt signaling and the evolution of embryonic posterior development. Curr Biol 19: R215-9.
88. Bolognesi R, Farzana L, Fischer TD, et al. 2008. Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol 18: 1624-9.
89. McGregor AP, Pechmann M, Schwager EE, et al. 2008. Wnt8 is required for growth-zone establishment and development of opisthosomal segments in a spider. Curr Biol 18: 1619-23.
90. Nakaya MA, Biris K, Tsukiyama T, et al. 2005. Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development 132: 5425-36.
91. Hayward P, Kalmar T, Arias AM. 2008. Wnt/Notch signalling and information processing during development. Development 135: 411-24.
92. Chipman AD, Arthur W, Akam M. 2004. Early development and segment formation in the centipede Strigamia maritima (Geophilomorpha). Evol Dev 6: 78-89.
93. Smith J, Davidson EH. 2008. Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo. Proc Natl Acad Sci U S A 105: 20089-94.
94. Vincent JP. 1998. Compartment boundaries: where, why and how? Int J Dev Biol 42: 311-5.
95. Larsen CW, Hirst E, Alexandre C, et al. 2003. Segment boundary formation in Drosophila embryos. Development 130: 5625-35.
96. Jacobs DK, Wray CG, Wedeen CJ, et al. 2000. Molluscan engrailed expression, serial organization, and shell evolution. Evol Dev 2: 340-7.
97. Gao F, Davidson EH. 2008. Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. Proc Natl Acad Sci U S A 105: 6091-6.
98. Arthur W, Jowett T, Panchen A. 1999. Segments, limbs, homology, and co-option. Evol Dev 1: 74-6.
99. Shubin N, Tabin C, Carroll S. 2009. Deep homology and the origins of evolutionary novelty. Nature 457: 818-23.
100. Shubin N, Tabin CJ, Carroll SB. 1997. Fossils, genes and the evolution of animal limbs. Nature 388: 639-48.