Larval apical sensory organ in a neritimorph gastropod, an ancient gastropod lineage with feeding larvae

Zoomorphology

Volumn 128, Issue 4, 2009, Pages 327-338

  Page, Louise R ^a   Kempf, S C ^b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b AUBURN UNIVERSITY   (United States)

Author keywords

Apical ganglion; Electron microscopy; Immunolabeling; Neurodevelopment; Planktotrophy

Indexed keywords

CAENOGASTROPODA; EUKARYOTA; GASTROPODA; NERITA; NERITOPSINA;

EID: 70350371454     PISSN: 0720213X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00435-009-0093-9     Document Type: Article

References (50)

1. Bandel K (1982) Morphologie und Bildung der frühontogenetischen Gehäuse bei conchiferen Mollusken. Facies 7:1-198. doi:10.1007/BF02537225.
2. Barlow LA, Truman JW (1992) Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone, Haliotis rufescens. J Neurobiol 23:829-844. doi:10.1002/neu.480230705.
3. Bonar DB (1978) Ultrastructure of a cephalic sensory organ in larvae of the gastropod Phestilla sibogae (Aeolidacea, Nudibranchia). Tissue Cell 10:153-165. doi:10.1016/0040-8166(78)90014-9.
4. Bourne GC (1908) Contributions to the morphology of the group Neritacea of aspidobranch gastropods. Part I. The Neritidae. Proc Zool Soc Lond 1908:810-887.
5. Byrne M, Nakajima Y, Chee FC, Burke RD (2007) Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol Dev 9:432-445.
6. Chia FS, Koss R (1981) Fine structural study of the statocysts in the veliger larva of the nudibranch, Rostanga pulchra. Cell Tissue Res 214:67-80. doi:10.1007/BF00235145.
7. Chia FS, Koss R (1984) Fine structure of the cephalic sensory organ in the larva of the nudibranch Rostanga pulchra (Mollusca, Opisthobranchia, Nudibranchia). Zoomorphology 104:131-139. doi:10.1007/BF00312131.
8. Colgan DJ, Ponder WF, Beacham E, Macaranas J (2007) Molecular phylogenetics of Caenogastropoda Gastropoda: Mollusca). Mol Phylogenet Evol 42:717-737. doi:10.1016/j.ympev.2006.10.009.
9. Conklin EG (1897) The embryology of Crepidula. J Morphol 13:1-226. doi:10.1002/jmor.1050130102.
10. Dickinson AJG, Croll RP (2003) Development of the larval nervous system of the gastropod Ilyanassa obsoleta. J Comp Neurol 466:197-218. doi:10.1002/cne.10863.
11. Dickinson AJG, Nason J, Croll RP (1999) Histochemical localization of FMRFamide, serotonin and catecholamine in embryonic Crepidula fornicata (Prosobranchia: Gastropoda). Zoomorphology 119:49-62. doi:10.1007/s004350050080.
12. Gifondorwa DJ, Leise EM (2006) Programmed cell death in the apical ganglion during larval metamorphosis of the marine mollusc Ilyanassa obsoleta. Biol Bull 210:109-120. doi:10.2307/4134600.
13. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum, New York, pp 26-60.
14. Hadfield MG, Miller SE (1987) On developmental patterns of opisthobranchs. Am Malacol Bull 5:197-214.
15. Hadfield MG, Strathmann MF, Strathmann RR (1997) Ciliary currents of non-feeding veligers in putative basal clades of gastropods. Invertebr Biol 116:313-321. doi:10.2307/3226863.
16. Hadfield MG, Meleshkevitch EA, Boudko DY (2000) The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol Bull 198:67-76. doi:10.2307/1542804.
17. Haszprunar G (1988) On the origin and evolution of major gastropod groups, with special reference to the Streptoneura. J Molluscan Stud 54:367-441. doi:10.1093/mollus/54.4.367.
18. Haszprunar G, Salvini-Plawen L, Rieger RM (1995) Larval planktotrophy: a primitive trait in the Bilateria? Acta Zool (Stockholm) 76:141-154.
19. Haszprunar G, Friedrich S, Wanninger A, Ruthensteiner B (2002) Fine structure and immunocytochemistry of a new chemosensory system in the chiton larva (Mollusca: Polyplacophora). J Morphol 251:210-218. doi:10.1002/jmor.1084/jmor.1084.
20. Hay Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond B Biol Sci 267:1071-1079. doi:10.1098/rspb.2000.1111.
21. Kano Y (2006) Usefulness of the opercular nucleus for inferring early development in neritimorph gastropods. J Morphol 267:1120-1136. doi:10.1002/jmor.10458.
22. Kempf SC, Page LR (2005) Anti-tubulin labeling reveals ampullary neuron ciliary bundles in opisthobranch larvae and a new putative neural structure associated with the apical ganglion. Biol Bull 208:169-182. doi:10.2307/3593149.
23. Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386:507-528. doi:10.1002/(SICI)1096-9861(19970929)386:3<507::AID-CNE12>3.0.CO;2 -7.
24. Lacalli TC (1994) Apical organs, epithelial domains, and the origin of the chordate nervous system. Am Zool 34:533-541.
25. LaForge NL, Page LR (2007) Development in Berthella californica (Gastropoda: Opisthobranchia) with comparative observations on phylogenetically relevant larval characters among nudipleuran opisthobranchs. Invertebr Biol 126:318-334. doi:10.1111/j.1744-7410.2007.000102.x.
26. Leise EM, Thavaradhara K, Durham NR, Turner BE (2001) Serotonin and nitric oxide regulate metamorphosis in the marine snail Ilyanassa obsoleta. Am Zool 41:258-267. doi:10.1668/0003-1569(2001)041[0258:SANORM]2.0.CO;2.
27. Lesoway MP, Page LR (2008) Growth and differentiation during delayed metamorphosis of feeding gastropod larvae: signatures of ancestry and innovation. Mar Biol (Berl) 153:723-734. doi:10.1007/s00227-007-0849-z.
28. Lin MF, Leise EM (1996) Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta. J Comp Neurol 374:180-193. doi:10.1002/(SICI)1096-9861(19961014)374:2<180::AID-CNE2>3.0.CO;2- Z.
29. Lindberg DR, Guralnick RP (2003) Phyletic patterns of early development in gastropod mollusks. Evol Dev 5:494-507. doi:10.1046/j.1525-142X.2003.03055.x.
30. Marois R, Carew TJ (1997a) Fine structure of the apical ganglion and its serotonergic cells in the larva of Aplysia californica. Biol Bull 192:388-398. doi:10.2307/1542748.
31. Marois R, Carew TJ (1997b) Ontogeny of serotonergic neurons in Aplysia californica. J Comp Neurol 386:477-490. doi:10.1002/(SICI)1096-9861(19970929)386:3<477::AID-CNE10>3.0.CO;2 -8.
32. Marois R, Carew TJ (1997c) Projection patterns and target tissues of the serotonergic cells in larval Aplysia californica. J Comp Neurol 386:491-506. doi:10.1002/(SICI)1096-9861(19970929)386:3<491::AID-CNE11>3.0.CO;2 -E.
33. B: immunolabeling of neurons in diverse invertebrates. J Comp Neurol 273:500-512. doi:10.1002/cne.902730406.
34. McArthur AG, Koop BF (1999) Partial 28S rDNA sequences and the antiquity of hydrothermal vent endemic gastropods. Mol Phylogenet Evol 13:255-274. doi:10.1006/mpev.1999.0645.
35. Nützel A, Lehnert O, Fryda J (2006) Origin of planktotrophy: evidence from early mollusks. Evol Dev 8:325-330. doi:10.1111/j.1525-142X.2006.00105.x.
36. Nützel A, Frýda J, Yancey TE, Anderson JR (2007) Larval shells of late Palaeozic naticopsid gastropods (Neritopsoidea: Neritimorpha) with a discussion of the early neritimorph evolution. Palaontologische Z 81:213-228.
37. Page LR (2002a) Apical sensory organ in larvae of the patellogastropod Tectura scutum. Biol Bull 202:6-22. doi:10.2307/1543218.
38. Page LR (2002b) Comparative structure of the larval apical sensory organ in gastropods and hypotheses about function and developmental evolution. Invertebr Reprod Dev 41:193-200.
39. Page LR, Parries SC (2000) Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 418:383-401. doi:10.1002/(SICI)1096-9861(20000320)418:4<383::AID-CNE2>3.0.CO;2- B.
40. Ponder WF, Lindberg DR (1997) Towards a phylogeny of gastropod mollusks: an analysis using morphological characters. Zool J Linn Soc 119:83-265. doi:10.1111/j.1096-3642.1997.tb00137.x.
41. Richardson KC, Jarrett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning for electron microscopy. Stain Technol 35:313-323.
42. Ruthensteiner B, Schaefer (2002) The cephalic sensory organ in veliger larvae of pulmonates (Gastropoda: Mollusca). J Morphol 251:93-102. doi:10.1002/jmor.1076.
43. Schaefer K, Ruthensteiner B (2001) The cephalic sensory organ in pelagic and intracapsular larvae of the primitive opisthobranch genus Haminoea (Mollusca: Gastropoda). Zool Anz 240:67-80. doi:10.1078/0044-5231-00007.
44. Scheltema RS (1971) Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biol Bull 140:284-322. doi:10.2307/1540075.
45. Spencer HG, Waters JM, Eichhorst TE (2007) Taxonomy and nomenclature of black nerites (Gastropoda: Neritimorpha: Nerita) from the South Pacific. Invertebr Syst 21:229-237. doi:10.1071/IS06038.
46. Thavaradhara K, Leise EM (2001) Loalization of nitric oxide synthase-like immunoreactivity in the developing nervous system of the snail Ilyanassa obsoleta. J Neurocytol 30:449-456. doi:10.1023/A:1015669112986.
47. Ulthe D (1995) Fine structure of the cephalic sensory organ in veliger larvae of Littorina littorea (L.) (Mesogastropoda, Littorinidae). Hydrobiologia 309:45-52. doi:10.1007/BF00014471.
48. Wagner PJ (2002) Phylogenetic relationships of the earliest anisostrophically coiled gastropods. Smithsonian Contributions to Paleobiology, no. 88. Smithsonian Institution Press, Washington DC.
49. Winnepenninckx B, Steiner G, Backeljau T, De Wachter R (1998) Details of gastropod phylogeny inferred from 18S rRNA sequences. Mol Phylogenet Evol 9:55-63. doi:10.1006/mpev.1997.0439.
50. Yoon SH, Kim W (2007) 18S Ribosomal DNA sequences provide insight into the phylogeny of patellogastropod limpets (Mollusca: Gastropoda). Mol Cells 23:64-71.