Evolutionary crossroads in developmental biology: Cyclostomes (lamprey and hagfish)

Development (Cambridge)

Volumn 139, Issue 12, 2012, Pages 2091-2099

  Shimeld, Sebastian M ^a   Donoghue, Phillip C J ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Cyclostome; Evolution; Gnathostome; Hagfish; Lamprey

Indexed keywords

MESSENGER RNA; MICRORNA;

ADAPTIVE IMMUNITY; ARTICLE; DEVELOPMENTAL BIOLOGY; EVOLUTION; FIN (ORGAN); GENE SILENCING; HAGFISH; JAW; LAMPREY; LIFE CYCLE; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; SKELETON; SOMITE; TRANSGENICS;

ANIMALS; BIOLOGICAL EVOLUTION; DEVELOPMENTAL BIOLOGY; HAGFISHES; LAMPREYS; LIFE CYCLE STAGES; MODELS, ANIMAL;

AGNATHA; GNATHOSTOMATA (VERTEBRATE); HAGFISH; PETROMYZONTIDAE; VERTEBRATA;

EID: 84861378543     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.074716     Document Type: Article

References (88)

1. Bajoghli, B., Guo, P., Aghaallaei, N., Hirano, M., Strohmeier, C., McCurley, N., Bockman, D. E., Schorpp, M., Cooper, M. D. and Boehm, T. (2011). A thymus candidate in lampreys. Nature 470, 90-94.
2. Bertrand, S. and Escriva, H. (2011). Evolutionary crossroads in developmental biology: amphioxus. Development 138, 4819-4830.
3. Boorman, C. J. and Shimeld, S. M. (2002). Cloning and expression of a Pitx homeobox gene from the lamprey, a jawless vertebrate. Dev. Genes Evol. 212, 349-353.
4. Bothe, I., Ahmed, M. U., Winterbottom, F. L., von Scheven, G. and Dietrich, S. (2007). Extrinsic versus intrinsic cues in avian paraxial mesoderm patterning and differentiation. Dev. Dyn. 236, 2397-2409.
5. Brazeau, M. D. (2009). The braincase and jaws of a Devonian 'acanthodian' and modern gnathostome origins. Nature 457, 305-308.
6. Cattell, M., Lai, S., Cerny, R. and Medeiros, D. M. (2011). A new mechanistic scenario for the origin and evolution of vertebrate cartilage. PLoS ONE 6, e22474.
7. Cerny, R., Cattell, M., Sauka-Spengler, T., Bronner-Fraser, M., Yu, F. and Medeiros, D. M. (2010). Evidence for the prepattern/cooption model of vertebrate jaw evolution. Proc. Natl. Acad. Sci. USA 107, 17262-17267.
8. Conel, J. L. (1931). The genital system of the Myxinoidea: A study based on notes and drawing of these organs in Bedellostomata made by Bashford Dean. In The Bashford Dean Memorial Volume, Archaic Fishes (ed. E. W. Gudger), pp. 67-102. New York: The American Museum of Natural History.
9. Dahn, R. D., Davis, M. C., Pappano, W. N. and Shubin, N. H. (2007). Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning. Nature 445, 311-314.
10. Dean, B. (1898). On the development of the Californian hag-fish, Bdellostoma stouti, Lockington. Quart. J. Microsc. Sci. 40, 269-279.
11. Dehal, P. and Boore, J. L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314.
12. Delarbre, C., Gallut, C., Barriel, V., Janvier, P. and Gachelin, G. (2002). Complete mitochondrial DNA of the hagfish, Eptatretus burgeri: the comparative analysis of mitochondrial DNA sequences strongly supports the cyclostome monophyly. Mol. Phylogenet. Evol. 22, 184-192.
13. Delsuc, F., Brinkmann, H., Chourrout, D. and Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965-968.
14. Derobert, Y., Baratte, B., Lepage, M. and Mazan, S. (2002). Pax6 expression patterns in Lampetra fluviatilis and Scyliorhinus canicula embryos suggest highly conserved roles in the early regionalization of the vertebrate brain. Brain Res. Bull. 57, 277-280.
15. Doflein, F. (1898). Bericht über eine wissenschaftliche Reise nach Californien. Sitzungsber Gesellsch Morph. Physiol. München 14, 105-118.
16. Donoghue, P. C. and Purnell, M. A. (2005). Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312-319.
17. Donoghue, P. C. and Sansom, I. J. (2002). Origin and early evolution of vertebrate skeletonization. Microsc. Res. Tech. 59, 352-372.
18. Donoghue, P. C. J., Forey, P. L. and Aldridge, R. J. (2000). Conodont affinity and chordate phylogeny. Biol. Rev. 75, 191-251.
19. Donoghue, P. C. J., Graham, A. and Kelsh, R. N. (2008). The origin and evolution of the neural crest. BioEssays 30, 530-541.
20. Fernholm, B. (1969). A third embryo of Myxine: considerations on hypophysial ontogeny and phylogeny. Acta Zool. 50, 169-177.
21. Freitas, R., Zhang, G. J. and Cohn, M. J. (2006). Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442, 1033-1037.
22. Furlong, R. and Holland, P. W. H. (2002). Bayesian phlogenetic analysis supports monophyly of Ambulacraria and Cyclostomes. Zool. Sci. 19, 593-599.
23. Gans, C. and Northcutt, R. G. (1983). Neural crest and the origin of the vertebrates: a new head. Science 220, 268-274.
24. Gillis, J. A., Dahn, R. D. and Shubin, N. H. (2009). Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. Proc. Natl. Acad. Sci. USA 106, 5720-5724.
25. Gorbman, A. (1997). Hagfish development. Zool. Sci. 14, 375-390.
26. Guo, P., Hirano, M., Herrin, B. R., Li, J., Yu, C., Sadlonova, A. and Cooper, M. D. (2009). Dual nature of the adaptive immune system in lampreys. Nature 459, 796-801.
27. Hammond, K. L., Baxendale, S., McCauley, D. W., Ingham, P. W. and Whitfield, T. T. (2009). Expression of patched, prdm1 and engrailed in the lamprey somite reveals conserved responses to Hedgehog signaling. Evol. Dev. 11, 27-40.
28. Hardisty, M. W. (2006). Lampreys: Life Without Jaws. Ceredigion: Forrest Text.
29. Hecht, J., Stricker, S., Wiecha, U., Stiege, A., Panopoulou, G., Podsiadlowski, L., Poustka, A. J., Dieterich, C., Ehrich, S., Suvorova, J. et al. (2008). Evolution of a core gene network for skeletogenesis in chordates. PLoS Genet. 4, e1000025.
30. Heimberg, A. M., Sempere, L. F., Moy, V. N., Donoghue, P. C. and Peterson, K. J. (2008). MicroRNAs and the advent of vertebrate morphological complexity. Proc. Natl. Acad. Sci. USA 105, 2946-2950.
31. Heimberg, A. M., Cowper-Sal-lari, R., Semon, M., Donoghue, P. C. and Peterson, K. J. (2010). microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc. Natl. Acad. Sci. USA 107, 19379-19383.
32. Hoffmann, F. G., Opazo, J. C. and Storz, J. F. (2011). Whole-genome duplications spurred the functional diversification of the Globin gene superfamily in vertebrates. Mol. Biol. Evol. 29, 303-312.
33. Holmgren, N. (1946). On two embryos of Myxine glutinosa. Acta Zool. 27, 1-90.
34. Horigome, N., Myojin, M., Ueki, T., Hirano, S., Aizawa, S. and Kuratani, S. (1999). Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev. Biol. 207, 287-308.
35. Inoue, J. G., Miya, M., Tsukamoto, K. and Nishida, M. (2003). Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the 'ancient fish'. Mol. Phylogenet. Evol. 26, 110-120.
36. Inoue, J. G., Miya, M., Lam, K., Tay, B.-H., Danks, J. A., Bell, J., Walker, T. I. and Venkatesh, B. (2010). Evolutionary origin and phylogeny of the modern Holocephalans (Chondrichthyes: Chimaeriformes): A mitogenomic perspective. Mol. Biol. Evol. 27, 2576-2586.
37. Jeffery, W. R., Strickler, A. G. and Yamamoto, Y. (2004). Migratory neural crestlike cells form body pigmentation in a urochordate embryo. Nature 431, 696-699.
38. Kaneto, S. and Wada, H. (2011). Regeneration of amphioxus oral cirri and its skeletal rods: implications for the origin of the vertebrate skeleton. J. Exp. Zool. B Mol. Dev. Evol. 316, 409-417.
39. Kuraku, S. and Kuratani, S. (2006). Timescale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zool. Sci. 23, 1053-1064.
40. Kuraku, S., Hoshiyama, D., Katoh, K., Suga, H. and Miyata, T. (1999). Monophyly of lampreys and hagfishes supported by nuclear DNA-coded genes. J. Mol. Evol. 49, 729-735.
41. Kuraku, S., Meyer, A. and Kuratani, S. (2009). Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Mol. Biol. Evol. 26, 47-59.
42. Kuraku, S., Takio, Y., Sugahara, F., Takechi, M. and Kuratani, S. (2010). Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. Dev. Biol. 341, 315-323.
43. Kuratani, S., Ueki, T., Hirano, S. and Aizawa, S. (1998). Rostral truncation of a cyclostome, Lampetra japonica, induced by all-trans retinoic acid defines the head/trunk interface of the vertebrate body. Dev. Dyn. 211, 35-51.
44. Kuratani, S., Nobusada, Y., Horigome, N., Myojin, M. and Hirano, S. (1999). Craniofacial development in the lamprey embryo and evolution of the vertebrate jaw. Am. Zool. 39, 140A.
45. Kusakabe, R., Tochinai, S. and Kuratani, S. (2003). Expression of foreign genes in lamprey embryos: An approach to study evolutionary changes in gene regulation. J. Exp. Zool. 296B, 87-97.
46. Langille, R. M. and Hall, B. K. (1988). Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lamprey, Petromyzon marinus (L). Development 102, 301-310.
47. Lemaire, P. (2011). Evolutionary crossroads in developmental biology: the tunicates. Development 138, 2143-2152.
48. McCauley, D. W. and Bronner-Fraser, M. (2006). Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441, 750-752.
49. McEwen, G. K., Goode, D. K., Parker, H. J., Woolfe, A., Callaway, H. and Elgar, G. (2009). Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet. 5, e1000762.
50. Murakami, Y., Ogasawara, M., Sugahara, F., Hirano, S., Satoh, N. and Kuratani, S. (2001). Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128, 3521-3531.
51. Murakami, Y., Pasqualetti, M., Takio, Y., Hirano, S., Rijli, F. M. and Kuratani, S. (2004). Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain. Development 131, 983-995.
52. Neidert, A. H., Virupannavar, V., Hooker, G. W. and Langeland, J. A. (2001). Lamprey Dlx genes and early vertebrate evolution. Proc. Natl. Acad. Sci. USA 98, 1665-1670.
53. Neyt, C., Jagla, K., Thisse, C., Thisse, B., Haines, L. and Currie, P. D. (2000). Evolutionary origins of vertebrate appendicular muscle. Nature 408, 82-86.
54. Nicholls, H. (2009). Evolution: Mouth to mouth. Nature 461, 164-166.
55. Nikitina, N., Sauka-Spengler, T. and Bronner-Fraser, M. (2008). Dissecting early regulatory relationships in the lamprey neural crest gene network. Proc. Natl. Acad. Sci. USA 105, 20083-20088.
56. Nikitina, N., Bronner-Fraser, M. and Sauka-Spengler, T. (2009). The sea lamprey petromyzon marinus. In Emerging Model Organisms, Vol. 1. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
57. Nohara, M., Nishida, M., Manthacitra, V. and Nishikawa, T. (2004). Ancient phylogenetic separation between Pacific and Atlantic cephalochordates as revealed by mitochondrial genome analysis. Zool. Sci. 21, 203-210.
58. Ogasawara, M., Shigetani, Y., Hirano, S., Satoh, N. and Kuratani, S. (2000). Pax1/Pax9-related genes in an agnathan vertebrate, Lampetra japonica: Expression pattern of LjPax9 implies sequential evolutionary events toward the gnathostome body plan. Dev. Biol. 223, 399-410.
59. Ogg, J. G., Ogg, G. and Gradstein, F. M. (2008). The Concise Geologic Timescale. Cambridge: Cambridge University Press.
60. Ohtani, K., Yao, T., Kobayashi, M., Kusakabe, R., Kuratani, S. and Wada, H. (2008). Expression of Sox and fibrillar collagen genes in lamprey larval chondrogenesis with implications for the evolution of vertebrate cartilage. J. Exp. Zool. B Mol. Dev. Evol. 310, 596-607.
61. Ota, K. G. and Kuratani, S. (2007). Cyclostome embryology and early evolutionary history of vertebrates. Integr. Comp. Biol. 47, 329-337.
62. Ota, K. G. and Kuratani, S. (2008). Developmental biology of hagfishes, with a report on newly obtained embryos of the Japanese inshore hagfish, Eptatretus burgeri. Zool. Sci. 25, 999-1011.
63. Ota, K. G., Kuraku, S. and Kuratani, S. (2007). Hagfish embryology with reference to the evolution of the neural crest. Nature 446, 672-675.
64. Ota, K. G., Fujimoto, S., Oisi, Y. and Kuratani, S. (2011). Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish. Nat. Commun. 2, 373.
65. Pancer, Z., Amemiya, C. T., Ehrhardt, G. R., Ceitlin, J., Gartland, G. L. and Cooper, M. D. (2004). Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430, 174-180.
66. Pancer, Z., Saha, N. R., Kasamatsu, J., Suzuki, T., Amemiya, C. T., Kasahara, M. and Cooper, M. D. (2005). Variable lymphocyte receptors in hagfish. Proc. Natl. Acad. Sci. USA 102, 9224-9229.
67. Piavis, G. W. (1971). Embryology. In The Biology Of Lampreys, Vol. 1 (ed. M. W. Hardisty and I. C. Potter), pp. 361 London - New York: Academic Press.
68. Pierce, M. L., Weston, M. D., Fritzsch, B., Gabel, H. W., Ruvkun, G. and Soukup, G. A. (2008). MicroRNA-183 family conservation and ciliated neurosensory organ expression. Evol. Dev. 10, 106-113.
69. Price, G. (1896). Some points in the development of a myxinoid (Bdellostoma stouti Lockington). Acta. Anz. 12 Suppl., 81-86.
70. Purnell, M. A. (2001). Scenarios, selection and the ecology of early vertebrates. In Major Events In Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics And Development (ed. P. E. Ahlberg), pp. 187-208. London: Taylor & Francis.
71. Putnam, N. H., Butts, T., Ferrier, D. E., Furlong, R. F., Hellsten, U., Kawashima, T., Robinson-Rechavi, M., Shoguchi, E., Terry, A., Yu, J. K. et al. (2008). The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071.
72. Rogozin, I. B., Iyer, L. M., Liang, L., Glazko, G. V., Liston, V. G., Pavlov, Y. I., Aravind, L. and Pancer, Z. (2007). Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat. Immunol. 8, 647-656.
73. Sauka-Spengler, T. and Bronner-Fraser, M. (2008). Insights from a sea lamprey into the evolution of neural crest gene regulatory network. Biol. Bull. 214, 303-314.
74. Sauka-Spengler, T., Meulemans, D., Jones, M. and Bronner-Fraser, M. (2007). Ancient evolutionary origin of the neural crest gene regulatory network. Dev. Cell 13, 405-420.
75. Shigetani, Y., Sugahara, F., Kawakami, Y., Murakami, Y., Hirano, S. and Kuratani, S. (2002). Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science 296, 1316-1319.
76. Smith, J. J., Antonacci, F., Eichler, E. E. and Amemiya, C. T. (2009). Programmed loss of millions of base pairs from a vertebrate genome. Proc. Natl. Acad. Sci. USA 106, 11212-11217.
77. Sugahara, F., Aota, S., Kuraku, S., Murakami, Y., Takio-Ogawa, Y., Hirano, S. and Kuratani, S. (2011). Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development 138, 1217-1226.
78. Swain, G. P., Jacobs, A. J., Frei, E. and Selzer, M. E. (1994). A method for in-situ hybridization in wholemounted lamprey brain-neurofilament expression in larvae and adults. Exp. Neurol. 126, 256-269.
79. Swalla, B. J. and Smith, A. B. (2008). Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos. Trans. R. Soc. B Biol. Sci. 363, 1557-1568.
80. Tahara, Y. (1988). Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool. Sci. 5, 109-118.
81. Tretjakoff, D. (1926). Die Wirbelsaüle des Neunauges. Anatomica Anzeiger B 61, 387-396.
82. Wada, H. (2010). Origin and genetic evolution of the vertebrate skeleton. Zoolog. Sci. 27, 119-123.
83. Wilson, M. V. H., Hanke, G. F. and Marss, T. (2007). Paired fins of jawless vertebrates and their homologies across the agnathan-gnathostome transition. In Major Transitions in Vertebrate Evolution (ed. J. Anderson and H.-D. Sues). Bloomington: Indiana University Press.
84. Woolfe, A., Goodson, M., Goode, D. K., Snell, P., McEwen, G. K., Vavouri, T., Smith, S. F., North, P., Callaway, H., Kelly, K. et al. (2005). Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 3, e7.
85. Young, G. C. (2010). Placoderms (armored fish): Dominant vertebrates of the devonian period. Annu. Rev. Earth Planet. Sci. 38, 523-550.
86. Yu, J. K., Meulemans, D., McKeown, S. J. and Bronner-Fraser, M. (2008). Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Res. 18, 1127-1132.
87. Zhang, G. and Cohn, M. J. (2006). Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates. Proc. Natl. Acad. Sci. USA 103, 16829-16833.
88. Zhang, G., Miyamoto, M. M. and Cohn, M. J. (2006). Lamprey type II collagen and Sox9 reveal an ancient origin of the vertebrate collagenous skeleton. Proc. Natl. Acad. Sci. USA 103, 3180-3185