Evolutionary diversification of secondary mechanoreceptor cells in tunicata

BMC Evolutionary Biology

Lucia Manni²  Paolo Burighel²  Fabio Gasparini²  Federico Caicci²  Thomas Stach¹  Francesca Rigon² 

[1] Institut für Biologie, AG Vergleichende Zoologie, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 2, D-10115, Berlin, Germany;Dipartimento di Biologia, Università degli Studi di Padova, via U. Bassi 58/B, I-35121, Padova, Italy

关键词: Sensory cells;    Oikopleura dioica;    Oikopleura albicans;    Cladistic analysis;   

Others  :  1087226
DOI  :  10.1186/1471-2148-13-112

 received in 2013-03-21, accepted in 2013-05-28,  发布年份 2013

【 摘 要 】

Background

Hair cells are vertebrate secondary sensory cells located in the ear and in the lateral line organ. Until recently, these cells were considered to be mechanoreceptors exclusively found in vertebrates that evolved within this group. Evidence of secondary mechanoreceptors in some tunicates, the proposed sister group of vertebrates, has recently led to the hypothesis that vertebrate and tunicate secondary sensory cells share a common origin. Secondary sensory cells were described in detail in two tunicate groups, ascidians and thaliaceans, in which they constitute an oral sensory structure called the coronal organ. Among thaliaceans, the organ is absent in salps and it has been hypothesised that this condition is due to a different feeding system adopted by this group of animals. No information is available as to whether a comparable structure exists in the third group of tunicates, the appendicularians, although different sensory structures are known to be present in these animals.

Results

We studied the detailed morphology of appendicularian oral mechanoreceptors. Using light and electron microscopy we could demonstrate that the mechanosensory organ called the circumoral ring is composed of secondary sensory cells. We described the ultrastructure of the circumoral organ in two appendicularian species, Oikopleura dioica and Oikopleura albicans, and thus taxonomically completed the data collection of tunicate secondary sensory cells. To understand the evolution of secondary sensory cells in tunicates, we performed a cladistic analysis using morphological data. We constructed a matrix consisting of 19 characters derived from detailed ultrastructural studies in 16 tunicate species and used a cephalochordate and three vertebrate species as outgroups.

Conclusions

Our study clearly shows that the circumoral ring is the appendicularian homologue of the coronal organ of other tunicate taxa. The cladistic analysis enabled us to reconstruct the features of the putative ancestral hair cell in tunicates, represented by a simple monociliated cell. This cell successively differentiated into the current variety of oral mechanoreceptors in the various tunicate lineages. Finally, we demonstrated that the inferred evolutionary changes coincide with major transitions in the feeding strategies in each respective lineage.

【 授权许可】

   
2013 Rigon et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Delsuc F, Brinkmann H, Chourrout D, Philippe H: Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006, 439(7079):965-968.
• [2]Delsuc F, Tsagkogeorga G, Lartillot N, Philippe H: Additional molecular support for the new chordate phylogeny. Genesis 2008, 46(11):592-604.
• [3]Caicci F, Degasperi V, Gasparini F, Zaniolo G, Del Favero M, Burighel P, Manni L: Variability of hair cells in the coronal organ of ascidians (Chordata, Tunicata). Can J Zool 2010, 88(6):567-578.
• [4]Mackie GO, Burighel P, Caicci F, Manni L: Innervation of ascidian siphons and their responses to stimulation. Can J Zool 2006, 84(8):1146-1162.
• [5]Manni L, Mackie GO, Caicci F, Zaniolo G, Burighel P: Coronal organ of ascidians and the evolutionary significance of secondary sensory cells in chordates. J Comp Neurol 2006, 495(4):363-373.
• [6]Caicci F, Burighel P, Manni L: Hair cells in an ascidian (Tunicata) and their evolution in chordates. Hear Res 2007, 231(1–2):63-72.
• [7]Caicci F, Gasparini F, Rigon F, Zaniolo G, Burighel P, Manni L: The oral sensory structures of thaliacea (Tunicata) and consideration of the evolution of hair cells in chordata. J Comp Neurol 2013. in press
• [8]Olsson R, Holmberg K, Lilliemarck Y: Fine structure of the brain and brain nerves of Oikopleura dioica (Urochordata, Appendicularia). Zoomorphology 1990, 110(1):1-7.
• [9]Fol H: Études sur les Appendiculaires du Détroit de Messine. Genève: Ramboz et Schuchardt; 1872.
• [10]Galt CP, Mackie GO: Electrical Correlates of Ciliary Reversal in Oikopleura. J Exp Biol 1971, 55(1):205-212.
• [11]Lohmann H: Erste Klasse der Tunicaten: Appendiculariae. In Handbuch der Zoologie. vol. 5. Edited by Kükenthal W, Krumbach T. Berlin, Leipzig: Walter de Gruyter; 1933:15-164. vol. 5
• [12]Bone Q, Ryan KP: The Langerhans receptor of Oikopleura (Tunicata: Larvacea). J Marine Biol Assoc UK 1979, 59(01):69-75.
• [13]Bone Q, Best ACG: Ciliated Sensory Cells in Amphioxus (Branchiostoma). J Mar Biol Assoc UK 1978, 58(02):479-486.
• [14]Lacalli TC, Hou S: A reexamination of the epithelial sensory cells of amphioxus (Branchiostoma). Acta Zool 1999, 80(2):125-134.
• [15]Lacalli TC: Sensory systems in amphioxus: a window on the ancestral chordate condition. Brain Behav Evol 2004, 64(3):148-162.
• [16]Stokes MD, Holland ND: Embryos and Larvae of a Lancelet, Branchiostoma floridae, from Hatching through Metamorphosis: Growth in the Laboratory and External Morphology. Acta Zool 1995, 76(2):105-120.
• [17]Lacalli TC, Gilmour THJ, Kelly SJ: The oral nerve plexus in amphioxus larvae: function, cell types and phylogenetic significance. Proc R Soc Lond B Biol Sci 1999, 266(1427):1461-1470.
• [18]Harrison FW, Ruppert EE: Hemichordata, Chaetognatha, and the invertebrate Chordates. New York, Chichester: Wiley-Liss; 1997.
• [19]Northcutt RG, Gans C: The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q Rev Biol 1983, 58(1):1-28.
• [20]O’Neill P, Mak SS, Fritzsch B, Ladher RK, Baker CV: The amniote paratympanic organ develops from a previously undiscovered sensory placode. Nat Commun 2012, 3:1041.
• [21]Schlosser G: Making senses development of vertebrate cranial placodes. Int Rev Cell Mol Biol 2010, 283:129-234.
• [22]Mazet F, Shimeld SM: Molecular evidence from ascidians for the evolutionary origin of vertebrate cranial sensory placodes. J Exp Zool B Mol Dev Evol 2005, 304(4):340-346.
• [23]Kourakis MJ, Newman-Smith E, Smith WC: Key steps in the morphogenesis of a cranial placode in an invertebrate chordate, the tunicate Ciona savignyi. Dev Biol 2010, 340(1):134-144.
• [24]Bassham S, Postlethwait JH: The evolutionary history of placodes: a molecular genetic investigation of the larvacean urochordate Oikopleura dioica. Development 2005, 132(19):4259-4272.
• [25]Manni L, Agnoletto A, Zaniolo G, Burighel P: Stomodeal and neurohypophysial placodes in Ciona intestinalis: insights into the origin of the pituitary gland. J Exp Zool B Mol Dev Evol 2005, 304(4):324-339.
• [26]Veeman MT, Newman-Smith E, El-Nachef D, Smith WC: The ascidian mouth opening is derived from the anterior neuropore: reassessing the mouth/neural tube relationship in chordate evolution. Dev Biol 2010, 344(1):138-149.
• [27]Mazet F, Hutt JA, Milloz J, Millard J, Graham A, Shimeld SM: Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate sensory placodes. Dev Biol 2005, 282(2):494-508.
• [28]Mazet F, Hutt JA, Millard J, Shimeld SM: Pax gene expression in the developing central nervous system of Ciona intestinalis. Gene Expr Patterns 2003, 3(6):743-745.
• [29]Graham A, Shimeld SM: The origin and evolution of the ectodermal placodes. J Anat 2013, 222(1):32-40.
• [30]Kozmik Z, Holland ND, Kreslova J, Oliveri D, Schubert M, Jonasova K, Holland LZ, Pestarino M, Benes V, Candiani S: Pax-Six-Eya-Dach network during amphioxus development: conservation in vitro but context specificity in vivo. Dev Biol 2007, 306(1):143-159.
• [31]Maddison DR, Maddison WP: MacClade 4: Analysis of phylogeny and character evolution. Version 4.08. 2005. http://www.macclade.org webcite
• [32]Pleijel F: On character coding for phylogeny reconstruction. Cladistics 1995, 11(3):309-315.
• [33]Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates; 2003.
• [34]Kottelat M: European freshwater fishes. Biologia 1997, 52:1-271.
• [35]Holland ND, Yu JK: Epidermal receptor development and sensory pathways in vitally stained amphioxus (Branchiostoma floridae). Acta Zool 2002, 83(4):309-319.
• [36]Braun CB, Northcutt RG: The lateral line system of hagfishes (Craniata: Myxinoidea). Acta Zool 1997, 78(3):247-268.
• [37]Yamada Y, Hama K: Fine structure of the lateral-line organ of the common eel. Anguilla japonica. Z Zellforsch Mikrosk Anat 1972, 124(4):454-464.
• [38]Metcalfe WK, Kimmel CB, Schabtach E: Anatomy of the posterior lateral line system in young larvae of the zebrafish. J Comp Neurol 1985, 233(3):377-389.
• [39]Williams JA, Holder N: Cell turnover in neuromasts of zebrafish larvae. Hear Res 2000, 143(1–2):171-181.
• [40]Burighel P, Lane NJ, Gasparini F, Tiozzo S, Zaniolo G, Carnevali MD, Manni L: Novel, secondary sensory cell organ in ascidians: in search of the ancestor of the vertebrate lateral line. J Comp Neurol 2003, 461(2):236-249.
• [41]Burighel P, Caicci F, Zaniolo G, Gasparini F, Degasperi V, Manni L: Does hair cell differentiation predate the vertebrate appearance? Brain Res Bull 2008, 75(2–4):331-334.
• [42]Manni L, Caicci F, Gasparini F, Zaniolo G, Burighel P: Hair cells in ascidians and the evolution of lateral line placodes. Evol Dev 2004, 6(6):379-381.
• [43]Bone Q: The biology of pelagic tunicates. Oxford: Oxford University Press; 1998.
• [44]Gillespie PG: Molecular machinery of auditory and vestibular transduction. Curr Opin Neurobiol 1995, 5(4):449-455.
• [45]Thurm U, Brinkmann M, Golz R, Lawonn P, Oliver D: The supramolecular basis of mechanoelectric transduction studied in concentric hair bundles of invertebrates. In From Structure to Information in Sensory Systems: Proceedings of the International School of Biophysics, Casamicciola, Napoli, Italy, 14–19 October 1996. Edited by Taddei-Ferretti C, Musio C. Singapore: World Sci Publ; 1998:228-236.
• [46]Burighel P, Caicci F, Manni L: Hair cells in non-vertebrate models: lower chordates and molluscs. Hear Res 2011, 273(1–2):14-24.
• [47]Fenaux R: The house of Oikopleura dioica (Tunicata, Appendicularia): Structure and functions. Zoomorphology 1986, 106(4):224-231.
• [48]Mackie GO, Burighel P: The nervous system in adult tunicates: current research directions. Can J Zool 2005, 83(1):151-183.
• [49]Stach T, Turbeville JM: Phylogeny of Tunicata inferred from molecular and morphological characters. Mol Phylogenet Evol 2002, 25(3):408-428.
• [50]Moreno TR, Rocha RM: Phylogeny of the Aplousobranchia (Tunicata: Ascidiacea). Rev Bras de Zool 2008, 25:269-298.
• [51]Govindarajan AF, Bucklin A, Madin LP: A molecular phylogeny of the Thaliacea. J Plank Res 2011, 33(6):843-853.
• [52]Tsagkogeorga G, Turon X, Hopcroft R, Tilak M, Feldstein T, Shenkar N, Loya Y, Huchon D, Douzery E, Delsuc F: An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evol Biol 2009, 9:187. BioMed Central Full Text
• [53]Turon X, Lopez-Legentil S: Ascidian molecular phylogeny inferred from mtDNA data with emphasis on the Aplousobranchiata. Mol Phylogenet Evol 2004, 33(2):309-320.
• [54]Zeng LY, Swalla BJ: Molecular phylogeny of the protochordates: chordate evolution. Can J Zool 2005, 83(1):24-33.
• [55]Tatian M, Lagger C, Demarchi M, Mattoni C: Molecular phylogeny endorses the relationship between carnivorous and filter-feeding tunicates (Tunicata, Ascidiacea). Zool Scripta 2011, 40(6):603-612.
• [56]Stach T, Braband A, Podsiadlowski L: Erosion of phylogenetic signal in tunicate mitochondrial genomes on different levels of analysis. Mol Phylogenet Evol 2010, 55(3):860-870.
• [57]Fiala-Médioni A: Filter-feeding ethology of benthic invertebrates (ascidians). IV. Pumping rate, filtration rate, filtration efficiency. Mar Biol 1978, 48(3):243-249.
• [58]Petersen JK, Svane I: Filtration rate in seven Scandinavian ascidians: implications of the morphology of the gill sac. Mar Biol 2002, 140(2):397-402.
• [59]Petersen JK: Ascidian suspension feeding. J Exp Mar Biol Ecol 2007, 342(1):127-137.
• [60]Burighel P, Cloney RA: Urochordata: Ascidiacea. In Microscopic Anatomy of the Invertebrates. Edited by Harrison FW, Ruppert EE. New York: Wiley-Liss; 1997:221-347.
• [61]Godeaux J, Bone Q, Braconnot JC: Anatomy of Thaliacea. In The biology of the pelagic tunicates. Edited by Bone Q. Oxford, New York, Tokyo: Oxford University Press; 1998:1-24.
• [62]Bone Q, Braconnot J, Ryan KP: On the pharyngeal feeding filter of the salp Pegea confoederata (Tunicata: Thaliacea). Acta Zool 1991, 77(1):55-60.
• [63]Flood PR: House formation and feeding behaviour of Fritillaria borealis (Appendicularia: Tunicata). Mar Biol 2003, 143(3):467-475.
• [64]Fenaux R: Anatomy and functional morphology of the Appendicularia. In The biology of pelagic tunicates. Edited by Bone Q. Oxford New york Tokyo: Oxford University Press; 1998:25-34.
• [65]Flood PR: Architecture of, and water circulation and flow rate in, the house of the planktonic tunicate Oikopleura labradoriensis. Mar Biol 1991, 111(1):95-111.