Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
REVIEW (Open Access)

How to make a protostome

Claus Nielsen
+ Author Affiliations
- Author Affiliations

Zoological Museum, The Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Denmark. Email: cnielsen@snm.ku.dk

Invertebrate Systematics 26(1) 25-40 https://doi.org/10.1071/IS11041
Submitted: 7 October 2011  Accepted: 9 February 2012   Published: 19 June 2012

Journal Compilation © CSIRO Publishing 2012 Open Access CC BY-NC-ND

Abstract

The origin and radiation of the major metazoan groups can be elucidated by phylogenomic studies, but morphological evolution must be inferred from embryology and morphology of living organisms. According to the trochaea theory, protostomes are derived from a holoplanktonic gastraea with a circumblastoporal ring of downstream-collecting compound cilia (archaeotroch) and a nervous system comprising an apical ganglion and a circumblastoporal nerve ring. The pelago-benthic life cycle evolved through the addition of a benthic adult stage, with lateral blastopore closure creating a tube-shaped gut. The archaeotroch became differentiated as prototroch, metatroch and telotroch in the (trochophora) larva, but was lost in the adult. The apical ganglion was lost in the adult, as in all neuralians. Paired cerebral ganglia developed from the first micromere quartet. The circumblastoporal nerve became differentiated into a pair of ventral nerve cords with loops around mouth (the anterior part of the blastopore) and anus. Almost all new information about morphology and embryology fits the trochaea theory. The predicted presence of a perioral loop of the blastoporal nerve ring has now been demonstrated in two annelids. Alternative ‘intercalation theories’ propose that planktotrophic larvae evolved many times from direct-developing ancestors, but this finds no support from considerations of adaptation.


References

Ackermann, C., Dorresteijn, A., and Fischer, A. (2005). Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). Journal of Morphology 266, 258–280.
Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta).Crossref | GoogleScholarGoogle Scholar |

Åkesson, B. (1967). The embryology of the polychaete Eunice kobiensis. Acta Zoologica (Stockholm) 48, 142–192.
The embryology of the polychaete Eunice kobiensis.Crossref | GoogleScholarGoogle Scholar |

Altenburger, A., Martinez, P., and Wanninger, A. (2011). Homeobox gene expression in Brachiopoda: the role of Not and Cdx in bodyplan patterning, neurogenesis, and germ layer specification. Gene Expression Patterns 11, 427–436.
Homeobox gene expression in Brachiopoda: the role of Not and Cdx in bodyplan patterning, neurogenesis, and germ layer specification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2itrnN&md5=890cc78a766fa66c9d87673e980c6778CAS |

Anderson, D. T. (1969). On the embryology of the cirripede crustaceans Tetraclita rosea (Krauss), Tetraclita purpurascens (Wood), Chthamalus antennatus (Darwin) and Chamaesipho columna (Spengler) and some considerations of crustacean phylogenetic relationships. Philosophical Transactions of the Royal Society B 256, 183–235.
On the embryology of the cirripede crustaceans Tetraclita rosea (Krauss), Tetraclita purpurascens (Wood), Chthamalus antennatus (Darwin) and Chamaesipho columna (Spengler) and some considerations of crustacean phylogenetic relationships.Crossref | GoogleScholarGoogle Scholar |

Boyer, B. C., Henry, J. J., and Martindale, M. Q. (1998). The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Developmental Biology 204, 111–123.
The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotFSjurk%3D&md5=3362f2e5aafa99d14a9369e0dc55fce1CAS |

Brinkmann, N., and Wanninger, A. (2009). Neurogenesis suggests independent evolution of opercula in serpulid polychaetes. BMC Evolutionary Biology 9, 270.
Neurogenesis suggests independent evolution of opercula in serpulid polychaetes.Crossref | GoogleScholarGoogle Scholar |

Burfield, S. T. (1927). L.M.B.C. Memoir 28: Sagitta. Proceedings and Transactions of the Liverpool Biological Society 41, 1–101.

Cather, J. N. (1967). Cellular interactions in the development of the shell gland of the gastropod, Ilyanassa. The Journal of Experimental Zoology 166, 205–223.
Cellular interactions in the development of the shell gland of the gastropod, Ilyanassa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c7is1Wltw%3D%3D&md5=8469007f5131062b020b4e7508bae92dCAS |

Child, C. M. (1900). The early development of Arenicola and Sternaspis. Archiv für Entwicklungsmechanik der Organismen 9, 587–723.
The early development of Arenicola and Sternaspis.Crossref | GoogleScholarGoogle Scholar |

Conklin, E. G. (1897). The embryology of Crepidula. Journal of Morphology 13, 1–226.
The embryology of Crepidula.Crossref | GoogleScholarGoogle Scholar |

Cuénot, L. (1940). Essai d’arbre généalogique du règne animal. Comptes Rendus Hébdomadaires des Séances de l’Académie des Sciences (Paris) 210, 196–199.

Damen, P., and Dictus, W. J. A. G. (1994). Cell lineage of the prototroch of Patella vulgata (Gastropoda, Mollusca). Developmental Biology 162, 364–383.
Cell lineage of the prototroch of Patella vulgata (Gastropoda, Mollusca).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3gtVGjug%3D%3D&md5=e8626c93b4a4d9335907df6214ea49baCAS |

Damen, P., and Dictus, W. J. A. G. (1996). Organiser role of the stem cell of the mesoderm in prototroch patterning in Patella vulgata (Mollusca, Gastropoda). Mechanisms of Development 56, 41–60.
Organiser role of the stem cell of the mesoderm in prototroch patterning in Patella vulgata (Mollusca, Gastropoda).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWhtL8%3D&md5=dce0e440d88a3a712fe9f0963966458dCAS |

Dautert, E. (1929). Die Bildung der Keimblätter von Paludina vivipara. Zoologische Jahrbücher. Anatomie 50, 433–496.

Delsman, H. C. (1914). Entwicklungsgeschichte von Littorina obtusata. Tijdschrift van het Nederlandsche Dierkundige Vereenigung, 2. Ser. 13, 170–340.

Delsman, H. C. (1916). Eifurchung und Keimblattbildung bei Scoloplos armiger O. F. Müller. Tijdschrift van het Nederlandsche Dierkundige Vereenigung, 2. Ser. 14, 383–498.

Dickinson, A. J. G., and Croll, R. P. (2003). Development of the larval nervous system of the gastropod Ilyanassa obsoleta. The Journal of Comparative Neurology 466, 197–218.
Development of the larval nervous system of the gastropod Ilyanassa obsoleta.Crossref | GoogleScholarGoogle Scholar |

Dickinson, A. J. G., Nason, J., and Croll, R. P. (1999). Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia). Zoomorphology 119, 49–62.
Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia).Crossref | GoogleScholarGoogle Scholar |

Dictus, W. J. A. G., and Damen, P. (1997). Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (Mollusca). Mechanisms of Development 62, 213–226.
Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (Mollusca).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitVKqt7Y%3D&md5=1710dd7d1adbcd85a65d7aa5565c40c9CAS |

Doncaster, L. (1902). On the development of Sagitta; with notes on the anatomy of the adult. Quarterly Journal of Microscopical Sciences. New Series 46, 351–395.

Dorresteijn, A. W. C. (1998). How do spiralian embryos accomplish cell diversity? Zoology (Jena, Germany) 100, 307–319.

Drew, G. A. (1899). Some observations on the habits, anatomy and embryology of members of the Protobranchia. Anatomischer Anzeiger 15, 493–519.

Ellis, I., and Kempf, S. C. (2011). Characterization of the central nervous system and various peripheral innervations during larval development of the oyster Crassostrea virginica. Invertebrate Biology 130, 236–250.
Characterization of the central nervous system and various peripheral innervations during larval development of the oyster Crassostrea virginica.Crossref | GoogleScholarGoogle Scholar |

Erwin, D. H., Laflamme, M., Tweedt, S. M., Sperling, E. A., Pisani, D., and Peterson, K. J. (2011). The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097.
The Cambrian conundrum: early divergence and later ecological success in the early history of animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2mu7jJ&md5=525397f9aaa6d92dfb084adbe9f493ebCAS |

Fernando, W. (1931). The origin of the mesoderm in the gastropod Viviparus. Proceedings of the Royal Society (London) B 107, 381–390.
The origin of the mesoderm in the gastropod Viviparus.Crossref | GoogleScholarGoogle Scholar |

Fioroni, P. (1970). Die organogenetische und transitorische Rolle der Vitellophagen in der Darmentwicklung von Galathea (Crustacea, Anomura). Zeitschrift für Morphologie der Tiere 67, 263–306.

Fischer, A. H. L., and Scholtz, G. (2010). Axogenesis in the stomatopod crustacean Gonodactylaceus falcatus (Malacostraca). Invertebrate Biology 129, 59–76.
Axogenesis in the stomatopod crustacean Gonodactylaceus falcatus (Malacostraca).Crossref | GoogleScholarGoogle Scholar |

Fraipont, J. (1887). Le genre Polygordius. Fauna und Flora des Golfes von Neapel 14, 1–125.

Fuchs, J., and Wanninger, A. (2008). Reconstruction of the neuromuscular system of the swimming-type larva of Loxosomella atkinsae (Entoprocta) as inferred by fluorescence labelling and confocal microscopy. Organisms, Diversity & Evolution 8, 325–335.
Reconstruction of the neuromuscular system of the swimming-type larva of Loxosomella atkinsae (Entoprocta) as inferred by fluorescence labelling and confocal microscopy.Crossref | GoogleScholarGoogle Scholar |

Galtsoff, P. S. (1964). The American oyster: Crassostrea virginica Gmelin. Fishery Bulletin 64, 1–480.

Gifondorwa, D. J., and Leise, E. M. (2006). Programmed cell death in the apical ganglion during larval metamorphosis of the marine mollusc Ilyanassa obsoleta. The Biological Bulletin 210, 109–120.
Programmed cell death in the apical ganglion during larval metamorphosis of the marine mollusc Ilyanassa obsoleta.Crossref | GoogleScholarGoogle Scholar |

Goette, A. (1902). ‘Lehrbuch der Zoologie.’ (Engelmann: Leipzig.)

Goulding, M. Q. (2009). Cell lineage of the Ilyanassa embryo: evolutionary acceleration of regional differentiation during early development. PLoS ONE 4, e5506.
Cell lineage of the Ilyanassa embryo: evolutionary acceleration of regional differentiation during early development.Crossref | GoogleScholarGoogle Scholar |

Grobben, K. (1908). Die systematische Einteilung des Tierreichs. Verhandlungen der Kaiserlich-Königlichen Zoologisch-Botanischen Gesellschaft in Wien 58, 491–511.

Hadfield, M. G., Meleshkevitch, E. A., and Boudko, D. Y. (2000). The apical sensory organ of a gastropod veliger is a receptor for settlement cues. The Biological Bulletin 198, 67–76.
The apical sensory organ of a gastropod veliger is a receptor for settlement cues.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7nt1yjtw%3D%3D&md5=e4589e6080376749bd14f6b7dea6cf64CAS |

Hammarsten, O. D. (1918). Beitrag zur Embryonalentwicklung der Malacobdella grossa (Müll.). Arbeiten aus dem Zootomischen Institut der Universität zu Stockholm 1, 1–96.

Harzsch, S. (2001). Neurogenesis in the crustacean ventral nerve cord: homology of neuronal stem cells in Malacostraca and Branchiopoda? Evolution & Development 3, 154–169.
Neurogenesis in the crustacean ventral nerve cord: homology of neuronal stem cells in Malacostraca and Branchiopoda?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FhslCisw%3D%3D&md5=ebc27360189684ae97099e150d450a3fCAS |

Haszprunar, G., and Wanninger, A. (2008). On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa and Mollusca. Acta Zoologica (Stockholm) 89, 137–148.
On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa and Mollusca.Crossref | GoogleScholarGoogle Scholar |

Hatschek, B. (1888). ‘Lehrbuch der Zoologie, 1. Lieferung (pp. 1–144.)’. (Gustav Fischer: Jena.)

Hatschek, B. (1891). ‘Lehrbuch der Zoologie, 3. Lieferung (pp. 305–432.)’. (Gustav Fischer: Jena.)

Hay-Schmidt, A. (1995). The larval nervous system of Polygordius lacteus Schneider, 1868 (Polygordiidae, Polychaeta): immunocytochemical data. Acta Zoologica (Stockholm) 76, 121–140.
The larval nervous system of Polygordius lacteus Schneider, 1868 (Polygordiidae, Polychaeta): immunocytochemical data.Crossref | GoogleScholarGoogle Scholar |

Heath, H. (1899). The development of Ischnochiton. Zoologische Jahrbücher. Anatomie 12, 567–656.

Hejnol, A. (2010). A twist in time—The evolution of spiral cleavage in the light of animal phylogeny. Integrative and Comparative Biology 50, 695–706.

Hejnol, A., Martindale, M. Q., and Henry, J. Q. (2007). High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. Developmental Biology 305, 63–76.
High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksV2ksrk%3D&md5=b73c11c6a5f9ffc37ee5863e924ccb2eCAS |

Henry, J. J., and Martindale, M. Q. (1998). Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus. Developmental Biology 201, 253–269.
Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVGnsr8%3D&md5=f409703ce7428e5b3be51f0a39eaf983CAS |

Henry, J. Q., Okusu, A., and Martindale, M. Q. (2004). The cell lineage of the polyplacophoran Chaetopleura apiculata: variation in the spiralian program and implications for molluscan evolution. Developmental Biology 272, 145–160.
The cell lineage of the polyplacophoran Chaetopleura apiculata: variation in the spiralian program and implications for molluscan evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFyhtrY%3D&md5=e5a46505b97727d3c26b190ab213c87eCAS |

Henry, J. Q., Hejnol, A., Perry, K. J., and Martindale, M. Q. (2007). Homology of ciliary bands in spiralian trochophores. Integrative and Comparative Biology 47, 865–871.
Homology of ciliary bands in spiralian trochophores.Crossref | GoogleScholarGoogle Scholar |

Henry, J., Collin, R., and Perry, K. J. (2010). The slipper snail, Crepidula: an emerging lophotrochozoan model system. The Biological Bulletin 218, 211–229.

Hertzler, P. L. (2002). Development of the mesendoderm in the dendrobranchiate shrimp Sicyonia ingentis. Arthropod Structure & Development 31, 33–49.
Development of the mesendoderm in the dendrobranchiate shrimp Sicyonia ingentis.Crossref | GoogleScholarGoogle Scholar |

Hertzler, P. L., and Clark, W. H. (1992). Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116, 127–140.
| 1:STN:280:DyaK3s7jtVOlsA%3D%3D&md5=7d2eaaf301d13017baddbd3aec3805d9CAS |

Hickman, V. V. (1963). The occurrence in Tasmania of the land nemertine, Geonemertes australiensis Dendy, with some account of its distribution, habits, variations and development. Papers and Proceedings of the Royal Society of Tasmania 97, 63–75.

Hiebert, L. S., Gavelis, G., von Dassow, G., and Maslakova, S. A. (2010). Five invaginations and shedding of the larval epidermis during development of the hoplonemertean Pantinonemertes californiensis (Nemertea: Hoplonemertea). Journal of Natural History 44, 2331–2347.
Five invaginations and shedding of the larval epidermis during development of the hoplonemertean Pantinonemertes californiensis (Nemertea: Hoplonemertea).Crossref | GoogleScholarGoogle Scholar |

Iwata, F. (1960). Studies on the comparative embryology of nemerteans with special reference to their interrelationships. Publications from the Akkeshi Marine Biological Station 10, 1–51.

Jägersten, G. (1972). ‘Evolution of the Metazoan Life Cycle.’ (Academic Press: London.)

Kocot, K. M., Cannon, J. T., Todt, C., Citarella, M. R., Kohn, A. B., Meyer, A., Santos, S. R., Schander, C., Moroz, L. L., Lieb, B., and Halanych, K. M. (2011). Phylogenomics reveals deep molluscan relationships. Nature 477, 452–456.
Phylogenomics reveals deep molluscan relationships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFers7fE&md5=c10b128b9a705d9e6cb1e36b7ecddb6bCAS |

Lacalli, T. C. (1982). The nervous system and ciliary band of Müller’s larva. Proceedings of the Royal Society (London) B 217, 37–58.
The nervous system and ciliary band of Müller’s larva.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s7ksVWjsA%3D%3D&md5=e148e21a188ff7e2c28019f0dc4e6e58CAS |

Lacalli, T. C. (1983). The brain and central nervous system of Müller’s larva. Canadian Journal of Zoology 61, 39–51.
The brain and central nervous system of Müller’s larva.Crossref | GoogleScholarGoogle Scholar |

Lacalli, T. C. (1984). Structure and organization of the nervous system in the trochophore larva of Spirobranchus. Philosophical Transactions of the Royal Society B 306, 79–135.
Structure and organization of the nervous system in the trochophore larva of Spirobranchus.Crossref | GoogleScholarGoogle Scholar |

Lambert, J. D. (2010). Developmental patterns in spiralian embryos. Current Biology 20, R72–R77.
Developmental patterns in spiralian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVegtb4%3D&md5=0b5a5973ee5dc117a9b94f37487dec96CAS |

Lillie, F. R. (1895). The embryology of the Unionidae. Journal of Morphology 10, 1–100.
The embryology of the Unionidae.Crossref | GoogleScholarGoogle Scholar |

Malakhov, V. V. (1990). Description of the development of Ascopodaria discreta (Coloniales, Barentsiidae) and discussion of the Kamptozoa status in the animal kingdom. Zoologicheskij Zhurnal 69, 20–30.

Malakhov, V. V. (1994). ‘Nematodes. Structure, Development, Classification, and Phylogeny.’ (Smithsonian Institution Press: Washington, DC.)

Marcus, E. (1939). Briozoários marinhos brasileiros III. Boletim da Faculdade de Filosofia, Ciências e Letras, Universidade de Sao Paulo. Zoologia 3, 111–354.

Maslakova, S. A. (2010a). Development to metamorphosis of the nemertean pilidium larva. Frontiers in Zoology 7, 30.
Development to metamorphosis of the nemertean pilidium larva.Crossref | GoogleScholarGoogle Scholar |

Maslakova, S. A. (2010b). The invention of the pilidium larva in an otherwise perfectly good spiralian phylum Nemertea. Integrative and Comparative Biology 50, 734–743.
The invention of the pilidium larva in an otherwise perfectly good spiralian phylum Nemertea.Crossref | GoogleScholarGoogle Scholar |

Maslakova, S. A., and von Döhren, J. (2009). Larval development with transitory epidermis in Paranemertes peregrina and other hoplonemerteans. The Biological Bulletin 216, 273–292.

Maslakova, S. A., Martindale, M. Q., and Norenburg, J. L. (2004). Fundamental properties of the spiralian development program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea). Developmental Biology 267, 342–360.
Fundamental properties of the spiralian development program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvV2hsbs%3D&md5=8f89f01900d712cdc09e7bd007a33d79CAS |

Mead, A. D. (1897). The early development of marine annelids. Journal of Morphology 13, 227–326.
The early development of marine annelids.Crossref | GoogleScholarGoogle Scholar |

Meisenheimer, J. (1901). Entwicklungsgeschichte von Dreissensia polymorpha Pall. Zeitschrift fur Wissenschartliche Zoologie 69, 1–137.

Meyer, N. P., and Seaver, E. (2010). Cell lineage and fate map of the primary somatoblast of the polychaete annelid Capitella teleta. Integrative and Comparative Biology 50, 756–767.
Cell lineage and fate map of the primary somatoblast of the polychaete annelid Capitella teleta.Crossref | GoogleScholarGoogle Scholar |

Meyer, N. P., Boyle, M. J., Martindale, M. Q., and Seaver, E. C. (2010). A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta. EvoDevo 1, 8.
A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta.Crossref | GoogleScholarGoogle Scholar |

Nielsen, C. (1971). Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9, 209–341.

Nielsen, C. (1979). Larval ciliary bands and metazoan phylogeny. Fortschritte in der Zoologischen Systematik und Evolutionsforschung 1, 178–184.

Nielsen, C. (2001). ‘Animal Evolution. Interrelationships of the Living Phyla’, 2nd edn. (Oxford University Press: Oxford.)

Nielsen, C. (2004). Trochophora larvae: cell-lineages, ciliary bands and body regions. 1. Annelida and Mollusca. The Journal of Experimental Zoology 302B, 35–68.
Trochophora larvae: cell-lineages, ciliary bands and body regions. 1. Annelida and Mollusca.Crossref | GoogleScholarGoogle Scholar |

Nielsen, C. (2005). Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. The Journal of Experimental Zoology 304B, 401–447.
Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion.Crossref | GoogleScholarGoogle Scholar |

Nielsen, C. (2009). How did indirect development with planktotrophic larvae evolve? The Biological Bulletin 216, 203–215.

Nielsen, C. (2012). ‘Animal Evolution. Interrelationships of the Living Phyla’, 3rd edn. (Oxford University Press: Oxford.)

Nielsen, C., and Nørrevang, A. (1985). The trochaea theory: an example of life cycle phylogeny. In ‘The Origins and Relationships of Lower Invertebrates.’ (Eds S. Conway Morris, J. D. George, R. Gibson and H. M. Platt.) pp. 28–41. (Oxford University Press: Oxford.)

Norenburg, J. L., and Stricker, S. A. (2002). Phylum Nemertea. In ‘Atlas of Marine Invertebrate Larvae’. (Ed. C. M. Young.) pp. 163–177. (Academic Press: San Diego, CA.)

Page, L. R., and Parries, S. C. (2000). Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. The Journal of Comparative Neurology 418, 383–401.
Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7nvF2rtg%3D%3D&md5=d73fbd2ff27302c69c48f83032822754CAS |

Page, L. R., and Pedersen, R. V. K. (1998). Transformation of phytoplanktivorous larvae into predatory carnivores during the development of Polynices lewisii (Mollusca, Caenogastropoda). Invertebrate Biology 117, 208–220.
Transformation of phytoplanktivorous larvae into predatory carnivores during the development of Polynices lewisii (Mollusca, Caenogastropoda).Crossref | GoogleScholarGoogle Scholar |

Rabinowitz, J. S., and Lambert, J. D. (2010). Spiralian quartet developmental potential is regulated by specific localization elements that mediate asymmetric RNA segregation. Development 137, 4039–4049.
Spiralian quartet developmental potential is regulated by specific localization elements that mediate asymmetric RNA segregation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVelsA%3D%3D&md5=e3c923dabfbc74977fbf0a64dd486ae1CAS |

Rawlinson, K. A. (2010). Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits. Frontiers in Zoology 7, 12.
Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits.Crossref | GoogleScholarGoogle Scholar |

Reid, D. G. (1989). The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae. Philosophical Transactions of the Royal Society B 324, 1–110.
The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae.Crossref | GoogleScholarGoogle Scholar |

Render, J. (1997). Cell fate maps in the Ilyanassa obsoleta embryo beyond the third division. Developmental Biology 189, 301–310.
Cell fate maps in the Ilyanassa obsoleta embryo beyond the third division.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsVGrt7k%3D&md5=d7fc379dbf43740cf2989d27ccf67e8bCAS |

Reuter, M., and Gustafsson, M. K. S. (1995). The flatworm nervous system: pattern and phylogeny. In ‘The Nervous System of Invertebrates: An Evolutionary and Comparative Approach’. (Ed. O. Breidbach.) pp. 25–59. (Birkhäuser: Basel.)

Rieger, V., Perez, Y., Müller, C. H. G., Lipke, E., Sombke, A., Hansson, B. S., and Harzsch, S. (2010). Immunohistochemical analysis and 3D reconstruction of the cephalic nervous system in Chaetognatha: insights into the evolution of an early bilaterian brain? Invertebrate Biology 129, 77–104.
Immunohistochemical analysis and 3D reconstruction of the cephalic nervous system in Chaetognatha: insights into the evolution of an early bilaterian brain?Crossref | GoogleScholarGoogle Scholar |

Rieger, V., Perez, Y., Müller, C. H. G., Lacalli, T., Hansson, B. S., and Harzsch, S. (2011). Development of the nervous system in hatchlings of Spadella cephaloptera (Chaetognatha), and implications for nervous system evolution in Bilateria. Development, Growth & Differentiation 53, 740–759.
Development of the nervous system in hatchlings of Spadella cephaloptera (Chaetognatha), and implications for nervous system evolution in Bilateria.Crossref | GoogleScholarGoogle Scholar |

Riisgård, H. U., Nielsen, C., and Larsen, P. S. (2000). Downstream collecting in ciliary suspension feeders: the catch-up principle. Marine Ecology Progress Series 207, 33–51.
Downstream collecting in ciliary suspension feeders: the catch-up principle.Crossref | GoogleScholarGoogle Scholar |

Rouse, G. W. (1999). Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biological Journal of the Linnean Society. Linnean Society of London 66, 411–464.
Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa.Crossref | GoogleScholarGoogle Scholar |

Rouse, G. W. (2000). The epitome of hand waving? Larval feeding and hypotheses of metazoan phylogeny. Evolution & Development 2, 222–233.
The epitome of hand waving? Larval feeding and hypotheses of metazoan phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7osVOisQ%3D%3D&md5=fdb7e77a60c3eb48dcda0ee603027282CAS |

Ruppert, E. E. (1978). A review of metamorphosis of turbellarian larvae. In ‘Settlement and Metamorphosis of Marine Invertebrate Larvae’. (Eds F. S. Chia and M. E. Rice.) pp. 65–81. (Elsevier: New York.)

Schierenberg, E. (2005). Unusual cleavage and gastrulation in a freshwater nematode: developmental and phylogenetic implications. Development Genes and Evolution 215, 103–108.
Unusual cleavage and gastrulation in a freshwater nematode: developmental and phylogenetic implications.Crossref | GoogleScholarGoogle Scholar |

Scholtz, G., and Edgecombe, G. D. (2006). The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Development Genes and Evolution 216, 395–415.
The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence.Crossref | GoogleScholarGoogle Scholar |

Schulze, J., and Schierenberg, E. (2009). Embryogenesis of Romanomermis culicivorax: an alternative way to construct a nematode. Developmental Biology 334, 10–21.
Embryogenesis of Romanomermis culicivorax: an alternative way to construct a nematode.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFamtr%2FE&md5=0834e0884aca2cd402df38b360eb45afCAS |

Schulze, J., and Schierenberg, E. (2011). Evolution of embryonic development in nematodes. EvoDevo 2, 18.
Evolution of embryonic development in nematodes.Crossref | GoogleScholarGoogle Scholar |

Segrove, F. (1941). The development of the serpulid Pomatoceros triqueter L. Quarterly Journal of Microscopical Sciences. New Series 82, 467–540.

Shimotori, T., and Goto, T. (2001). Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: relationship to protostomes. Development, Growth & Differentiation 43, 371–382.
Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: relationship to protostomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fislaktw%3D%3D&md5=c34bcc2668f64bd6426813eb6414159aCAS |

Sly, B. J., Snoke, M. S., and Raff, R. A. (2003). Who came first – larvae or adults? Origins of bilaterian metazoan larvae. The International Journal of Developmental Biology 47, 623–632.

Smart, T. I., and Von Dassow, G. (2009). Unusual development of the mitraria larva in the polychaete Owenia collaris. The Biological Bulletin 217, 253–268.

Smith, J. E. (1935). The early development of the nemertean Cephalothrix rufifrons. Quarterly Journal of Microscopical Sciences. New Series 77, 335–381.

Smith, S. A., Wilson, N. G., Goetz, F. E., Feehery, C., Andrade, S. C. S., Rouse, G. W., Giribet, G., and Dunn, C. W. (2011). Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature 480, 364–367.
Resolving the evolutionary relationships of molluscs with phylogenomic tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOmsrnJ&md5=4d11b8f047fffb4d70f7cfcf1d62f909CAS |

Steinmetz, P. R. H., Kostyuchenko, R. P., Fischer, A., and Arendt, D. (2011). The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evolution & Development 13, 72–79.
The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii.Crossref | GoogleScholarGoogle Scholar |

Sulston, J. E., Schierenberg, E., White, J. G., and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100, 64–119.
The embryonic cell lineage of the nematode Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c%2FgsFCltQ%3D%3D&md5=b11273d47d774ed2960e192c57419d71CAS |

Thompson, T. E. (1960). The development of Neomenia carinata Tullberg (Mollusca Aplacophora). Proceedings of the Royal Society (London) B 153, 263–278.
The development of Neomenia carinata Tullberg (Mollusca Aplacophora).Crossref | GoogleScholarGoogle Scholar |

Treadwell, A. L. (1901). Cytogeny of Podarke obscura Verrill. Journal of Morphology 17, 399–486.
Cytogeny of Podarke obscura Verrill.Crossref | GoogleScholarGoogle Scholar |

Ulrich, W. (1951). Vorschläge zu einer Revision der Grosseinteilung des Tierreichs. Zoologischer Anzeiger 15, 244–271.

van den Biggelaar, J., and Dictus, W. J. A. G. (2004). Gastrulation in the molluscan embryo. In ‘Gastrulation. From Cells to Embryo’. (Ed. C. D. Stern.) pp. 63–77. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.)

Verdonk, N. H., and van den Biggelaar, J. A. M. (1983). Early development and the formation of the germ layers. In ‘The Mollusca, Vol. 3’. (Ed. K. M. Wilbur.) pp. 91–122. (Academic Press: New York.)

von Döhren, J. (2011). The fate of the larval epidermis in the Desor-larva of Lineus viridis (Pilidiophora, Nemertea) displays a historically constrained functional shift from planktotrophy to lecithotrophy. Zoomorphology 130, 189–196.
The fate of the larval epidermis in the Desor-larva of Lineus viridis (Pilidiophora, Nemertea) displays a historically constrained functional shift from planktotrophy to lecithotrophy.Crossref | GoogleScholarGoogle Scholar |

Voronezhskaya, E. E., Tyurin, S. A., and Nezlin, L. P. (2002). Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). The Journal of Comparative Neurology 444, 25–38.
Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora).Crossref | GoogleScholarGoogle Scholar |

Voronezhskaya, E. E., Nezlin, L. P., Odintsova, N. A., Plummer, J. T., and Croll, R. P. (2008). Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphology 127, 97–110.
Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia).Crossref | GoogleScholarGoogle Scholar |

Wanninger, A. (2009). Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the Tetraneuralia concept. The Biological Bulletin 216, 293–306.

Wanninger, A., Fuchs, J., and Haszprunar, G. (2007). Anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications. Invertebrate Biology 126, 268–278.
Anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications.Crossref | GoogleScholarGoogle Scholar |

Weisblat, D. A., Kim, S. Y., and Stent, G. S. (1984). Embryonic origins of cells in the leech Helobdella triserialis. Developmental Biology 104, 65–85.
Embryonic origins of cells in the leech Helobdella triserialis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3jslSnsg%3D%3D&md5=986c687d8876e35b1eb3682f53ded0d6CAS |

White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society B 314, 1–340.
The structure of the nervous system of the nematode Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rgvFejtA%3D%3D&md5=8c8d1c819f1272bdb839f82b0fe7c1afCAS |

Wierzejski, A. (1905). Embryologie von Physa fontinalis L. Zeitschrift fur Wissenschartliche Zoologie 83, 502–706.

Wilson, D. P. (1932). On the mitraria larva of Owenia fusiformis Delle Chiaje. Philosophical Transactions of the Royal Society B 221, 231–334.
On the mitraria larva of Owenia fusiformis Delle Chiaje.Crossref | GoogleScholarGoogle Scholar |

Woltereck, R. (1902). Trochophora-Studien I. Histologie der Larve und die Entstehung des Annelids bei den Polygordius-Arten der Nordsee. Zoologica (Stuttgart) 13, 1–71.

Woltereck, R. (1904a). Beiträge zur praktischen Analyse der Polygordius-Entwicklung nach dem “Nordsee-” und dem “Mittelmeer-Typus”. Archiv für Entwicklungsmechanik der Organismen 18, 377–403.
Beiträge zur praktischen Analyse der Polygordius-Entwicklung nach dem “Nordsee-” und dem “Mittelmeer-Typus”.Crossref | GoogleScholarGoogle Scholar |

Woltereck, R. (1904b). Wurm“kopf”, Wurmrumpf und Trochophora. Zoologischer Anzeiger 28, 273–322.

Wray, G. A. (1996). Parallel evolution of nonfeeding larvae in echinoids. Systematic Biology 45, 308–322.
Parallel evolution of nonfeeding larvae in echinoids.Crossref | GoogleScholarGoogle Scholar |

Xiao, S., and Laflamme, M. (2009). On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. Trends in Ecology & Evolution 24, 31–40.
On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota.Crossref | GoogleScholarGoogle Scholar |

Zardus, J. D., and Morse, M. P. (1998). Embryogenesis, morphology and ultrastructure of the pericalymma larva of Acila castrensis (Bivalvia: Protobranchia: Nuculoida). Invertebrate Biology 117, 221–244.
Embryogenesis, morphology and ultrastructure of the pericalymma larva of Acila castrensis (Bivalvia: Protobranchia: Nuculoida).Crossref | GoogleScholarGoogle Scholar |