Development of the nervous system in Phoronopsis harmeri (Lophotrochozoa, Phoronida) reveals both deuterostome- and trochozoan-like features

BMC Evolutionary Biology

Andreas Wanninger¹  Elena Temereva² 

[1] Dept. of Integrative Zoology, University of Vienna, Althanstr 14, 1090, Vienna, Austria;Department of Invertebrate Zoology, Biological faculty, Moscow State University, Moscow, 119991, Russia

关键词: Last common lophotrochozoan ancestor;    Ventral nerve cord;    Phylogeny;    Evolution;    Neurogenesis;   

Others  :  1140777
DOI  :  10.1186/1471-2148-12-121

 received in 2012-02-21, accepted in 2012-06-06,  发布年份 2012

【 摘 要 】

Background

Inferences concerning the evolution of invertebrate nervous systems are often hampered by the lack of a solid data base for little known but phylogenetically crucial taxa. In order to contribute to the discussion concerning the ancestral neural pattern of the Lophotrochozoa (a major clade that includes a number of phyla that exhibit a ciliated larva in their life cycle), we investigated neurogenesis in Phoronopsis harmeri, a member of the poorly studied Phoronida, by using antibody staining against serotonin and FMRFamide in combination with confocal microscopy and 3D reconstruction software.

Results

The larva of Phoronopsis harmeri exhibits a highly complex nervous system, including an apical organ that consists of four different neural cell types, such as numerous serotonin-like immunoreactive flask-shaped cells. In addition, serotonin- and FMRFamide-like immunoreactive bi- or multipolar perikarya that give rise to a tentacular neurite bundle which innervates the postoral ciliated band are found. The preoral ciliated band is innervated by marginal serotonin-like as well as FMRFamide-like immunoreactive neurite bundles. The telotroch is innervated by two neurite bundles. The oral field is the most densely innervated area and contains ventral and ventro-lateral neurite bundles as well as several groups of perikarya. The digestive system is innervated by both serotonin- and FMRFamide-like immunoreactive neurites and perikarya. Importantly, older larvae of P. harmeri show a paired ventral neurite bundle with serial commissures and perikarya.

Conclusions

Serotonin-like flask-shaped cells such as the ones described herein for Phoronopsis harmeri are found in the majority of lophotrochozoan larvae and therefore most likely belong to the ground pattern of the last common lophotrochozoan ancestor. The finding of a transitory paired ventral neurite bundle with serially repeated commissures that disappears during metamorphosis suggests that such a structure was part of the “ur-phoronid” nervous system, but was lost in the adult stage, probably due to its acquired sessile benthic lifestyle.

【 授权许可】

   
2012 Temereva and Wanninger; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Cohen B, Weydmann A: Molecular evidence that phoronids are a subtaxon of brachiopods (Brachiopoda: Phoronata) and that genetic divergence of metazoan phyla began long before the early Cambrian. Organisms Divers Evol 2005, 5:253-273.
• [2]Santagata S, Cohen B: Phoronid phylogenetics (Brachiopoda; Phoronata): evidence from morphological cladistics, small and large subunit rDNA sequences, and mitochondrial cox1. Zool J Linn Soc 2009, 157:34-50.
• [3]Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hillis DM, Lake JA: Evidence from 18 S ribosomal DNA that the lophophorates are protostome animals. Science 1995, 267:1641-1643.
• [4]Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock ShD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G: Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
• [5]Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW: Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci 2009, 276:4261-4270.
• [6]Hyman LH: Phoronida. In The invertebrates. Volume 5. Smaller coelomate groups. Edited by Boell EJ. McGraw-Hill, New York; 1959:228-274.
• [7]Siewing R: Das Archicoelomatenkonzept. Zool Jahrb Anat Ontog 1980, 103:439-482.
• [8]Temereva EN, Malakhov VV: Embryogenesis in phoronids. Invert Zool 2012, 9(1):1-39.
• [9]Altenburger A, Wanninger A: Neuromuscular development in Novocrania anomala: evidence for the presence of serotonin and a spiralian-like apical organ in lecithotrophic brachiopod larvae. Evol Dev 2010, 12(1):16-24.
• [10]Temereva EN, Malakhov VV: Embryogenesis and larval development of Phoronopsis harmeri Pixell, 1912 (Phoronida): dual origin of the coelomic mesoderm. Invert Reprod Dev 2007, 50:57-66.
• [11]Temereva EN, Malakhov VV: Organization of the epistome in Phoronopsis harmeri (Phoronida) and consideration of the coelomic organization in Phoronida. Zoomorphol 2011, 130:121-134.
• [12]Nielsen C: Animal phylogeny in the light of the trochaea theory. Biol J Linn Soc 1985, 25:243-299.
• [13]Nielsen C: Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. J Exp Zool (Mol Dev Evol) 2005, 304B:401-447.
• [14]Harzsch S: Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phyologeny. Integr Comp Biol 2006, 46:162-195.
• [15]Hay-Schmidt A: The nervous system of the actinotroch larva of Phoronis muelleri (Phoronida). Zoomorphol 1989, 108:333-351.
• [16]Hay-Schmidt A: Distribution of catecholamine containing, serotonin-like and neuropeptide FMRFamide-like immunoreactive neurons and processes in the nervous system of the actinotroch larva of Phoronis muelleri (Phoronida). Cell Tiss Res 1990, 259:105-118.
• [17]Hay-Schmidt A: Catecholamine-containing, serotonin-lake and FMRFamide-like immunoreactive neurons and processes in the nervous system of the early actinotroch larva of Phoronis vancouverensis (Phoronida): distribution and development. Can J Zool 1990, 68(7):1525-1536.
• [18]Lacalli TC: Structure and organization of the nervous system in the actinotroch larva of Phoronis vancouverensis. Phil Trans Roy Soc L 1990, 327:655-685.
• [19]Santagata S: Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol Dev 2002, 4:28-42.
• [20]Santagata S: Larval development of Phoronis pallida (Phoronida): implications for morphological convergence and divergence among larval body plans. J Morphol 2004, 259:347-358.
• [21]Santagata S, Zimmer RL: Comparison of the neuromuscular system among actinotroch larvae: systematic and evolutionary implication. Evol Dev 2002, 4:43-54.
• [22]Temereva EN: Ventral nerve cord in Phoronopsis harmeri larvae. J Exp Zool (Mol Dev Evol) 2012, 318B:26-34.
• [23]Temereva EN: The digestive tract of actinotroch larvae (Lophotrochozoa, Phoronida): anatomy, ultrastructure, innervations, and some observations of metamorphosis. Can J Zool 2010, 88(2):1149-1168.
• [24]Hay-Schmidt A: The evolution of the serotonergic nervous system. Proc R Soc L 2000, 267:1071-1079.
• [25]Voronezhskaya EE, Tyurin SA, Nezlin LP: Neuronal development in larval chiton Ischnochiton hakodadensis(Mollusca: Polyplacophora). J Comp Neurol 2002, 444:25-38.
• [26]Wanninger A: Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa. Acta Biol Hung 2008, 59(Suppl):127-136.
• [27]Wanninger A: Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the tetraneuralia concept. Biol Bull 2009, 216:293-306.
• [28]Voronezhskaya EE, Tsitrin EB, Nezlin LP: Neuronal development in larval Polychaete Phyllodoce maculate (Phyllodocidae). J Comp Neurol 2003, 455:299-309.
• [29]McDougall C, Chen W-Ch, Shimeld SM, Ferrier Dek: The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Front Zool 2006., 3(16) BioMed Central Full Text
• [30]Nezlin LP: The golden age of comparative morphology: laser scanning microscopy and neurogenesis in trochophore animals. Russ J Dev Biol 2010, 41(6):381-390.
• [31]Hay-Schmidt A: The larval nervous system of Polygordius lacteus Scheinder 1868 (Polygordiidae, Polychaeta): immunocytochemical data. Acta Zool 1995, 76:121-140.
• [32]Dickinson AJG, Croll RP: Development of the larval nervous system of the gastropod Ilyanassa obsoleta. J Comp Neurol 2003, 466:197-218.
• [33]Voronezhskaya EE, Nezlin LP, Odintsova NA: Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphol 2008, 127:97-110.
• [34]Kristof A, Klussmann-Kolb A: Neuromuscular development of Aeolidiella stephanieae Valdéz, 2005 (Mollusca, Gastropoda, Nudibranchia). Front Zool 2010., 7(5) http://www.frontiersinzoology.com/content/7/1/5 webcite
• [35]Rawlinson KA: Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits. Front Zool 2010., 7(12) http://www.frontiersinzoology.com/content/7/1/12 webcite
• [36]Nielsen C, Worsaae K: Structure and occurrence of cyphonautes larvae (Bryozoa, Ectoprocta). J Morphol 2010, 2010(271):1094-1109.
• [37]Santagata S: Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol Bull 2008, 215:3-23.
• [38]Santagata S, Resh C, Hejnol A, Martindale MQ, Passamaneck YJ: Development of the larval anterior neurogenic domains of Terebratalia transversa (Brachiopoda) provides insights into the diversification of larval apical organs and the spiralian nervous system. EvoDevo 2012., 3(3) BioMed Central Full Text
• [39]Altenburger A, Wanninger A: Comparative larval myogenesis and adult myoanatomy in the rhynchonelliform (articulate) brachiopods Argyrotheca cordata, A. cistellula, and Terebratalia transversa. Front Zool 2009, 6(3):14.
• [40]Wanninger A, Koop D, Degnan BM: Immunocytochemistry of the larval nervous system of Triphyllozoon mucronatum (Ectoprocta: Gymnolaemata: Cheilostomata) and its fate during metamorphosis. Zoomorphol 2005, 124:161-170.
• [41]Brinkmann N, Wanninger A: Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol Dev 2008, 10:606-618.
• [42]Altenburger A, Martinez P, Wanninger A: Homeobox gene expression in Brachiopoda: the role of Not and Cdx in bodyplan patterning, neurogenesis, and germ layer specification. Gene Expres Patt 2011, 11:427-436.
• [43]Beer AJ, Moss C, Thorndyke M: Development of serotonin-like and SALMFamide-like immunoreactivity in the nervous system of the sea urchin Psammechinus miliaris. Biol Bull 2001, 200(3):268-280.
• [44]Nielsen C, Hay-Schmidt A: Development of the Enteropneust Ptychodera flava: ciliary bands and nervous system. J Morphol 2007, 268:551-570.
• [45]Nezlin LP, Yushin VV: Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphol 2004, 123:1-13.
• [46]Temereva EN: New data on distribution, morphology and taxonomy of phoronid larvae (Phoronida, Lophophorata). Invert Zool 2009, 6(1):47-64.
• [47]Byrne M, Nakajima Y, Chee FC, Burke RD: Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol Dev 2007, 9:432-445.
• [48]Burke RD: Deuterostomy neuroanatome and the body plan paradox. Evol Dev 2011, 13(1):110-115.
• [49]Murabe N, Hatoyama H, Hase S, Komatsu MK, Burke RD, Kaneko H, Nakajima Y: Neural architecture of the brachiolaria larva of the starfish, Asterina pectinifera. J Comp Neur 2008, 509:271-282.
• [50]Dupont S, Thorndyke W, Thorndyke MC, Burke RD: Neural development of the brittlestar Amphiura filiformis. Dev Genes Evol 2009, 219:159-166.