How did indirect development with planktotrophic larvae evolve?

Biological Bulletin

Volumn 216, Issue 3, 2009, Pages 203-215

  Nielsen, Claus ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DEVELOPMENTAL BIOLOGY; EVOLUTIONARY THEORY; INVERTEBRATE; LARVA; LIFE CYCLE; SPECIALIZATION;

ANIMAL; ARTICLE; EVOLUTION; FEEDING BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; INVERTEBRATE; METAMORPHOSIS; ZOOPLANKTON;

ANIMALS; EVOLUTION; FEEDING BEHAVIOR; INVERTEBRATES; METAMORPHOSIS, BIOLOGICAL; ZOOPLANKTON;

EUMETAZOA; INVERTEBRATA;

EID: 67650979558     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/25548155     Document Type: Article

References (122)

1. Arendt, D., U. Technau, and J. Wittbrodt. 2001. Evolution of the bilaterian larval foregut. Nature 409: 81-85.
2. Baguñà, J., P. Martinez, J. Paps, and M. Riutort. 2008a. Back in time: a new systematic proposal for the Bilateria. Philos. Trans. R. Soc. bond. B 363: 1481-1491.
3. Baguñà, J., P. Martinez, J. Paps, and M. Riutort. 2008b. Unravelling body plan and axial evolution in the Bilateria with molecular phylo-genetic markers. Pp. 217-238 in Evolving Pathways. Key Themes in Evolutionary Developmental Biology, A. Minelli and G. Fusco, eds. Cambridge University Press, Cambridge.
4. Bailey, J. V., S. B. Joye, K. Kalanetra, B. E. Flood, and F. A. Corsetti. 2007. Evidence of giant sulphur bacteria in Neoproterozoic phosphorites. Nature 445: 198-201.
5. Baum, D. A., S. D. Smith, and S. S. Donovan. 2005. The tree-thinking challenge. Science 310: 979-980.
6. Bengtson, S., and G. Budd. 2004. Comment on "Small bilaterian fossils from 40 to 55 million years before the Cambrian." Science 306: 1291 a.
7. Bengtson, S., and Y. Zhao. 1997. Fossilized metazoan embryos from the Earliest Cambrian. Science 277: 1645-1648.
8. Bishop, C. D., D. F. Erezyilmaz, T. Flatt, C. D. Georgiou, M. G. Hadlitld, A. Heyland, J. Hodin, M. W. Jacobs, S. A. Maslakova, A. Pires, et al. 2006. What is metamorphosis? Integr. Comp. Biol. 46: 655-661.
9. Bonik, K., M. Grasshoff, and W. F. Gutmann. 1976. Die Evolution der Tierkonstruktionen. Natur Mus. 106: 129-143.
10. Bourlat, S. J., C. Nielsen, A. E. Lockyer, D. T. J. Littlewood, and M. J. Telford. 2003. Xenoturbella is a deuterostome that eats molluscs. Nature 424: 925-928.
11. Boyer, B. C, J. J. Henry, and M. Q. Martindale. 1998. The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev. Biol. 204: 111-123.
12. Buckland-Nicks, J., G. Gibson, and R. Koss. 2002. Phylum Mollusca: Gastropoda. Pp. 261-287 in Atlas of Marine Invertebrate Larvae, C. M. Young, ed. Academic Press, San Diego.
13. Butterfield, N. J. 2007. Macroevolution and macroecology through deep time. Palaeontology 50: 41-55.
14. Byrne, M., Y. Nakajima, F. C. Chee, and R. D. Burke. 2007. Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol. Dev. 9: 432-445.
15. Chen, J.-Y., P. Oliveri, C. W. Li, G. Q. Zhou, F. Gao, J. W. Hagadorn, K. J. Peterson, and E. H. Davidson. 2000. Precambrian animal diversity: putative phosphatized embryos from the Doushanto Formation of China. Proc. Natl. Acad. Sci. USA 97: 4457-4462.
16. Chen, J.-Y., D. J. Bottjer, P. Oliveri, S. Q. Dornbos, F. Gao, S. Ruffins, H. Chi, C. W. Li, and E. H. Davidson. 2004a. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science 305: 218-222.
17. Chen, J.-Y., P. Oliveri, E. Davidson, and D. J. Bottjer. 2004b. Response to comment on "Small bilaterian fossils from 40 to 55 million years before the Cambrian." Science 306: 1291b.
18. Collin, R. 2004. Phylogenetic effects, the loss of complex characters, and the evolution of development in calyptraeid gastropods. Evolution 58: 1488-1502.
19. Collins, A. G. 2002. Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J. Evol. Biol. IS: 418-432.
20. Collins, A. G., P. Schuchert, A. C. Marques, T. Jankowski, M. Medina, and B. Schierwater. 2006. Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and assessment of the utility of phylogenetic mixture methods. Syst. Biol. 55: 97-115.
21. Cook, C. E., E. Jiménez, M. Akam, and E. Saló. 2004. The Hox gene complement of acoel flatworms, a basal bilaterian clade. Evol. Dev. 6: 154-163.
22. Degnan, S. M., and B. M. Degnan. 2006. The origin of the pelago- benthic metazoan life cycle: What's sex to do with it? Integr. Comp. Biol. 46: 683-690.
23. Dewel, R. A. 2000. Colonial origin for Eumetazoans: major morphological transitions and the origin of bilaterian complexity. J. Morphol. 243: 35-74.
24. Doncaster, L. 1902. On the development of Sagitta; with notes on the anatomy of the adult. Q. J. Microsc. Sci. 46: 351-395.
25. Donoghue, P. C. J. 2007. Embryonic identity crisis. Nature 445: 155- 156.
26. Dunn, C. W., A. Hejnol, D. Q. Matus, K. Pang, W. E. Browne, S. A. Smith. E. C. Seaver, G. W. Rouse, M. Obst, G. D. Edgecombe, etal. 2008. Broad phylogenotrtic sampling improves resolution of the animal tree of life. Nature 452: 745-749.
27. Emlet, R. B. 1991. Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. Am. Zool. 31: 707-725.
28. Ereskovsky, A. V., and A. K. Dondua. 2006. The problem of germ layers in sponges (Porifera) and some issues concerning early metazoan evolution. Zool. Anz. 245: 65-76.
29. Fadlallah, Y. H. 1983. Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2: 129-150.
30. Fioroni, P. 1966. Zur Morphologie und Embryogenese des Darmtraktus
31. und der transistorischen Organe bei Prosobranchiem (Mollusca, Gastropoda). Rev. Suisse Zool. 73: 621-876.
32. Freeman, G., and J. W. Lundelius. 2005. The transition from plank-totrophy to lecithotrophy in larvae of Lower Palaeozoic rhynchonelli-form brachiopods. Lethaia 38: 219-254.
33. Freeman, G., and J. W. Lundelius. 2007. Origin of planktotrophy evidence from early molluscs: a response to Nutzel et al. (2006). Evol. Dev. 9: 307-310.
34. ricke, H. W. 1970. Neue kriechende Ctenophoren der Gattung Coelo- plana aus Madagaskar. Mar. Biol. 5: 225-238.
35. Garcia-Fernandez, G. 2005. The genesis and evolution of the ho- meobox gene clusters. Nat. Rev. Genet. 6: 881-892.
36. Garstang, W. 1928. The morphology of the Tunicata, and its bearings on the phylogeny of the Chordata. Q. J. Microsc. Sci. 72: 51-187.
37. Giribet, G., C. W. Dunn, G. D. Edgecombe, and G. W. Rouse. 2007. A modern look at the animal tree of life. Zootaxa 1668: 61-79.
38. Goreau, N. I., T. J. Goreau, and R. L. Hayes. 1981. Settling survivorship and spatial aggregation in planulae and juveniles of the coral Porites porites (Pallas). Bull. Mar. Sci. 31: 424-435.
39. Gostling, N. J., C.-W. Thomas, J. M. Greenwood, X. Dong, S. Bengt- son, E. C. Raff, R. A. Raff, B. M. Degnan, M. Stampanoni, and P. C. J. Donoghue. 2008. Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy. Evol. Dev. 10: 339-349.
40. Göltze, E. 1938. Bau und Leben von Caecum glabrum (Montagu). Zool. Jahrb. Syst. 71: 55-122.
41. Grimson, A., M. Srivastava, B. Fahey, B. J. Woodcroft, H. R. Chiang, N. King, B. M. Degnan, D. S. Rokhsar, and D. P. Bartel. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs
42. in animals. Nature 455: 1193-1197.
43. Hadfield, K. A., B. J. Swalla, and W. R. Jeffery. 1995. Multiple origins of anural development in ascidians inferred from rDNA sequences. J. Mol. Evol. 40: 413-427.
44. Haeckel, E. 1874. Die Gastraea-Theorie, die phylogenetische Classification des Thierreichs und die Homologie der Keimblatter. Jena. Zeitschr. Naturw. 8: 1-55. 1 pi.
45. Hatschek, B. 1888. Lehrbuch der Zoologie, I. Lieferung (pp. 1-144). Gustav Fischer, Jena.
46. Hatschek, B. 1891. Lehrbuch der Zoologie, 3. Lieferung (pp. 305-432). Gustav Fischer, Jena.
47. Hejnol, A., and M. Q. Martindale. 2008. Acoel development supports a simple planula-like urbilaterian. Philos. Trans. R. Soc. Lond. B 363: 1493-1501.
48. Holley, M. C, and G. A. B. Shelton. 1984. Reversal of the direction of mucus-flow on the ciliated pharynx of a sea anemone. J. Exp. Biol. 108: 151-161.
49. Huber, J. L., K. B. da Silva, W. R. Bates, and B. J. Swalla. 2000. The evolution of anural larvae in molgulid ascidians. Semin. Cell Dev. Biol. 11: 419-426.
50. Hyman, L. H. 1951. The Invertebrates, Vol. 2, Platyhelminthes and Rhynchocoela. The Acoelomate Bilateria. McGraw-Hill, New York.
51. Jägersten, G. 1959. Further remarks on the early phylogeny of the Metazoa. Zool. Bidr. Upps. 33: 79-108.
52. Jägersten, G. 1972. Evolution of the Metazoan Life Cycle. Academic Press, London.
53. Lacalli, T. C. 1993. Ciliary bands in echinoderm larvae: evidence for structural homologies and a common plan. Acta Zool. 74: 127-133.
54. Lartillot, N., and H. Philippe. 2008. Improvement of molecular phylogenetic inference and the phylogeny of the Bilateria. Philos. Trans. R. Soc. Lond. B 363: 1463-1472.
55. Lemons, D., and N. McGinnis. 2006. Genomic evolution of Hox clusters. Science 313: 1918-1922.
56. Lin, J.-P., A. C. Scott, C.-W. Li, H.-J. Wu, W. I. Ausich, Y.-L. Zhao, and Y.-K. Hwu. 2006. Silicified egg clusters from a Middle Cambrian Burgess Shale-type deposit, Guizhou, south China. Geology 34: 1037-1040.
57. Love, A. C, A. E. Lee, M. E. Andrews, and R. A. Raff. 2008. Co- option and dissociation in larval origins and evolution: the sea urchin larval gut. Evol. Dev. 10: 74-88.
58. Martin, V. J., and R. Koss. 2002. Phylum Cnidaria. Pp. 51-108 in Atlas of Marine Invertebrate Larvae, C. Young, ed. Academic Press, San Diego.
59. Maslakova, S. A., M. Q. Martindale, and J. L. Norenburg. 2004. Vestigial prototroch in a basal nemertean. Carinoma tremaphoros (Nemertea; Palaeonemertea). Evol. Dev. 6: 219-226.
60. Matus, D. Q., K. Pang, H. Marlow, C. W. Dunn, G. H. Thomsen, and M. Q. Martindale. 2006. Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc. Natl. Acad. Sci. USA 103: 11195-11200.
61. McEdward, L. R., and D. A. Janies. 1993. Life cycle evolution in asteroids: What is a larva? Biol. Bull. 184: 255-268.
62. Mortensen, T. 1912. Ctenophora. Pp. 1-96, 10 pis. in The Danish Ingolf Expedition, Vol. 5A(2). Bianco Luno, Copenhagen.
63. Nakano, H., T. Hibino, T. Oji, Y. Hara, and S. Amemiya. 2003. Larval stages of a living sea lily (stalked crinoid echinoderm). Nature 421: 158-160.
64. Nielsen, C. 1971. Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9: 209-341.
65. Nielsen, C. 1979. Larval ciliary bands and metazoan phylogeny. Fortschr. Zool. Syst. Evolforsch. 1: 178-184.
66. Nielsen, C. 1998. Origin and evolution of animal life cycles. Biol. Rev. 73: 125-155.
67. Nielsen, C. 1999. Origin of the chordate central nervous system and the origin of the chordates. Dev. Genes Evol. 209: 198-205.
68. Nielsen, C. 2000. The origin of metamorphosis. Evol. Dev. 2: 127-129. Nielsen, C. 2001. Animal Evolution: Interrelationships of the Living Phyla, 2nd ed. Oxford University Press, Oxford.
69. Nielsen, C. 2004. Trochophora larvae: cell-lineages, ciliary bands and body regions. 1. Annelida and Mollusca. J. Exp. Zool. (Mol. Dev. Evol.) 302B: 35-68.
70. Nielsen, C. 2005. Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. J. Exp. Zool. (Mol. Dev. Evol.) 304B: 401-447.
71. Nielsen, C. 2008a. Ontogeny of the spiralian brain. Pp. 399-416 in Evolving Pathways: Key Themes in Evolutionary Developmental Biology, A. Minelli and G. Fusco, eds. Cambridge University Press, Cambridge.
72. Nielsen, C. 2008b. Six major steps in animal evolution: Are we derived sponge larvae? Evol. Dev. 10: 241-257.
73. Nielsen, C. 2009. Some aspects of spiralian development. Acta Zool. (In press).
74. Nielsen, C, and P. Martinez. 2003. Patterns of gene expression: homology or homocracy? Dev. Genes Evol. 213: 149-154.
75. Olive, P. J. W. 1985. Covariability of reproductive traits in marine invertebrates: implications for the phylogeny of the lower invertebrates. Pp. 42-59 in The Origins and Relationships of Lower Invertebrates, S. Conway Morris, ed. Oxford University Press, Oxford.
76. Pernet, B. 2003. Persistent ancestral feeding structures in nonfeeding annelid larvae. Biol. Bull. 205: 295-307.
77. Pernet, B., P. Y. Qian, G. Rouse, C. M. Young, and K. J. Eckelbarger. 2002. Phylum Annelida: Polychaeta. Pp. 209-243 in Atlas of Marine Invertebrate Larvae, C. M. Young, ed. Academic Press, San Diego.
78. Peterson, K. J., and E. H. Davidson. 2000. Regulatory evolution and the origin of the bilaterians. Proc. Natl. Acad. Sci. USA 97: 4430- 4433.
79. Peterson, K. J., R. A. Cameron, and E. H. Davidson. 2000. Bilaterian origins: significance of new experimental observations. Dev. Biol. 219: 1-17.
80. Peterson, K. J., M. A. McPeek, and D. A. D. Evans. 2005. Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular data. Paleobiology 31(Suppl. 2): 36-55.
81. Peterson, K. J., J. A. Cotton, J. G. Gehling, and D. Pisani. 2008. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos. Trans. R. Soc. Lond. B 363: 1435-1443.
82. Raff, E. C, E. M. Popodi, B. J. Sly, R. Turner, J. T. Villinksi, and R. A. Raff. 1999. A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 126: 1937- 1945.
83. Raff, E. C, E. M. Popodi, J. S. Kauffman, B. J. Sly, F. R. Turner, V. B. Morris, and R. A. Raff. 2003. Regulatory punctuated equilibrium and convergence in the evolution of developmental pathways in direct- developing sea urchins. Evol. Dev. 5: 478-493.
84. Raff, R. A. 2008. Origins of the other metazoan body plans: the evolution of larval forms. Philos. Trans. R. Soc. Lond. B 363: 1473-1479.
85. Ramachandra, N. B., R. D. Gates, P. Ladurner, D. K. Jacobs, and V. Hartenstein. 2002. Embryonic development in the primitive bilaterian Neochildia fusca: normal morphogenesis and isolation of POU genes Brn-I and Brn-2. Dev. Genes Evol. 212: 55-69.
86. Reeve, M. R., and M. A. Walter. 1978. Nutritional ecology of cteno- phores-a review of recent research. Adv. Mar. Biol. 15: 249-287.
87. Reid, D. G. 1990. A cladistic phylogeny of the genus Littorina (Gastropoda): implications for evolution of reproductive strategies and for classification. Hydrobiologia 193: 1-19.
88. Reid, D. G. 1996. Systematics and Evolution of Littorina. Ray Society, London.
89. Rentsch, F., R. Anton, M. Saina, M. Hammerschmidt, T. W. Holstein, and U. Technau. 2006. Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev. Biol. 296: 375-387.
90. Rieger, R. M. 1994. The biphasic life-cycle-a central theme of metazoan evolution. Am. Zool. 34: 484-491.
91. Riisgard, H. U., C. Nielsen, and P. S. Larsen. 2000. Downstream collecting in ciliary suspension feeders: the catch-up principle. Mar. Ecol. Prog. Ser. 207: 33-51.
92. Rouse, G. 2000a. Bias? What bias? The evolution of downstream larval- feeding in animals. Zool. Scr. 29: 213-236.
93. Rouse, G. 2000b. Polychaetes have evolved feeding larvae numerous times. Bull. Mar. Sci. 67: 391-409.
94. Rouse, G. W. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol. J. Linn. Soc. 66: 411-464.
95. Rouse, G. W., and F. Pleijel. 2001. Polychaetes. Oxford University Press, Oxford.
96. Ruiz-Trillo, I., J. Paps, M. Loukota, C. Ribera, U. Jondelius, J. Baguñà, and M. Riutort. 2002. A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemerto- dermatida are basal bilaterians. Proc. Natl. Acad. Sci. USA 99: 11246- 11251.
97. Runnegar, B. 2007. No evidence for planktotrophy in Cambrian molluscs. Evol. Dev. 9: 311-312.
98. Ruppert, E. E. 1997. Cephalochordata (Acrania). Pp. 349-504 in Microscopic Anatomy of Invertebrates, Vol. 15, F. W. Harrison, ed. Wiley-Liss, New York.
99. Ruppert, E. E., R. S. Fox, and R. D. Barnes. 2004. Invertebrate Zoology: A Functional Evolutionary Approach (7th ed. of R. D. Barnes' Invertebrate Zoology). Brooks/Cole, Belmont. CA.
100. Salvini-Plawen, L. v. 1978. On the origin and evolution of the lower Metazoa. Z. Zool. Syst. Evohitionsforsch. 16: 40-88.
101. Salvini-Plawen, L. v. 1980. Was ist eine Trochophora? Eine Analyse der Larventypen mariner Protostomier. Zool. Jahrb. Anat. 103: 389-423.
102. Schwalm, F. E. 1997. Arthropods: the Insects. Pp. 259-278 in Embryology. Constructing the Organism, S. F. Gilbert and A. M. Raunio, eds. Sinauer Associates, Sunderland, MA.
103. Schwarz, J. A., W. M. Weis, and D. C. Potts. 2002. Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Mar. Biol. 140: 471-478.
104. Sempere, L. F., P. Martinez, C. Cole, J. Baguñà, and K. J. Peterson. 2007. Phylogenetic distribution of microRNAs supports the basal position of acoel flatworms and the polyphyly of Platyhelminthes. Evol. Dev. 9: 409-415.
105. Sewell, M. A., and F. S. McEuen. 2002. Phylum Echinodermata: Ho-lothuroidea. Pp. 513-530 in Atlas of Marine Invertebrate Larvae, CM. Young, ed. Academic Press, San Diego.
106. Shankland, M., and R. M. Savage. 1997. Annelids, the segmented worms. Pp. 219-235 in Embryology. Constructing the Organism, S. F. Gilbert and A. M. Raunio, eds. Sinauer Associates, Sunderland, MA.
107. Sly, B. J., M. S. Snoke, and R. A. Raff. 2003. Who came first-larvae or adults? Origins of bilaterian metazoan larvae. Int. .1. Dev. Biol. 47: 623-632.
108. Smith, M. J., J. D. G. Boom, and R. A. Raff. 1990. Single-copy DNA distance between two congeneric sea urchin species exhibiting radically different modes of development. Mol. Biol. Evol. 7: 315-326.
109. Sperling, E. A., D. Pisani, and K. J. Peterson. 2007. Poriferan paraphyly and its implications for Precambrian paleobiology. Pp.
110. 355-368 in The Rise and Fall of the Ediacaran Biota, P. Vickers-Rich and P. Komarower. eds. Special Publication 286. The Geological Society of London.
111. Srivastava, M., E. Begovic, J. Chapman, N. H. Putnam, U. Hellsten, T. Kawashima, A. Kuo, T. Mitros, A. Salamov, M. L. Carpenter, et al. 2008. The Trichoplax genome and the nature of placozoans. Nature 454: 955-960.
112. Strathmann, R. R. 2007. Time and extent of ciliary response to particles in a non-filtering feeding mechanism. Biol. Bull. 212: 93-103.
113. Sulston, J. E., E. Schierenberg, J. G. White, and J. N. Thomson. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100: 64-119.
114. Swalla, B. J., and W. R. Jeffery. 1996. Requirement of the Manx gene for expression of chordate features in a tailless ascidian larva. Science 274: 1205-1208.
115. Wang, X., and D. V. Lavrov. 2007. Mitochondrial genome of the homoscleromorph Oscarella carmela (Porifera, Demospongiae) re veals unexpected complexity in the common ancestor of sponges and other animals. Mo! Biol. Evol. 24: 363-373.
116. Werner, B. 1984. Stamm Cnidaria, Nesseltiere. Pp. 11-305 in A. Kaest- ner's Lehrbuch der Speziellen Zoologie, 4th ed., H. E. Gruner, ed. Gustav Fischer, Stuttgart.
117. Willmer, P. 1990. Invertebrate Relationships. Patterns in Animal Evolution. Cambridge University Press, Cambridge.
118. Wolpert, L. 1999. From egg to adult to larva. Evol. Dev. 1: 3-4.
119. Wray, G. A. 1995. Punctuated evolution of embryos. Science 267: 1115-1116.
120. Wray, G. A. 1996. Parallel evolution of nonfeeding larvae in echinoids. Syst. Biol. 45: 308-322.
121. Wray, G. A. 2000. The evolution of embryonic patterning mechanisms in animals. Semin. Cell Dev. Biol. 11: 385-393.
122. Xiao, S., and A. H. Knoll. 2000. Phosphatized animal embryos from the Neoproterozoic Doushanto Formation at Weng'an. Guizhou, South China. J. Paleont. 74: 767-788.