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Evo-Devo: Non-model Species in Cell and Developmental Biology pp 63–105Cite as

Oikopleura dioica: An Emergent Chordate Model to Study the Impact of Gene Loss on the Evolution of the Mechanisms of Development

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Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 68))

Abstract

The urochordate Oikopleura dioica is emerging as a nonclassical animal model in the field of evolutionary developmental biology (a.k.a. evo-devo) especially attractive for investigating the impact of gene loss on the evolution of mechanisms of development. This is because this organism fulfills the requirements of an animal model (i.e., has a simple and accessible morphology, a short generation time and life span, and affordable culture in the laboratory and amenable experimental manipulation), but also because O. dioica occupies a key phylogenetic position to understand the diversification and origin of our own phylum, the chordates. During its evolution, O. dioica genome has suffered a drastic process of compaction, becoming the smallest known chordate genome, a process that has been accompanied by exacerbating amount of gene losses. Interestingly, however, despite the extensive gene losses, including entire regulatory pathways essential for the embryonic development of other chordates, O. dioica retains the typical chordate body plan. This unexpected situation led to the formulation of the so-called inverse paradox of evo-devo, that is, when a genetic diversity is able to maintain a phenotypic unity. This chapter reviews the biological features of O. dioica as a model animal, along with the current data on the evolution of its genes and genome. We pay special attention to the numerous examples of gene losses that have taken place during the evolution of this unique animal model, which is helping us to understand to which the limits of evo-devo can be pushed off.

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References

  • Acuña JL, Kiefer M (2000) Functional response of the appendicularian Oikopleura dioica. Limnol Oceanogr 45:608–618

    Article  Google Scholar 

  • Acuña JL, Bedo AW, Harris RP, Anadón R (1995) The seasonal succession of appendicularians (Tunicata: Appendicularia) off Plymouth. J Mar Biol Assoc UK 75:755–758

    Article  Google Scholar 

  • Acuña JL, Deibel D, Saunders P, Booth B, Hatfield E, Klein B, Mei ZP, Rivkin R (2002) Phytoplankton ingestion by appendicularians in the North Water. Deep Sea Res Part II Top Stud Oceanogr 49:5101–5115

    Article  Google Scholar 

  • Albalat R (2009) The retinoic acid machinery in invertebrates: ancestral elements and vertebrate innovations. Mol Cell Endocrinol 313:23–35

    Article  CAS  PubMed  Google Scholar 

  • Albalat R, Cañestro C (2016) Evolution by gene loss. Nat Rev Genet 17:379–391

    Article  CAS  PubMed  Google Scholar 

  • Albalat R, Martí-Solans J, Cañestro C (2012) DNA methylation in amphioxus: from ancestral functions to new roles in vertebrates. Brief Funct Genomics 11:142–155

    Article  CAS  PubMed  Google Scholar 

  • Alldredge AL (2005) The contribution of discarded appendicularian houses to the flux of particulate organic carbon from oceanic surface waters. In: Gorsky G, Youngbluth MJ, Deibel D (eds) Response of marine ecosystems to global change: ecological impact of appendicularians. Éditions Scientifiques, Paris

    Google Scholar 

  • Almazán A, Ferrández-Roldán A, Albalat R, Cañestro C (2019) Developmental atlas of appendicularian Oikopleura dioica actins provides new insights into the evolution of the notochord and the cardio-paraxial muscle in chordates. Dev Biol 448:260–270

    Article  PubMed  CAS  Google Scholar 

  • Aravena GP, Palma S (2002) Taxonomic identification of appendicularians collected in the epipelagic waters off northern Chile (Tunicata, Appendicularia). Rev Chilena Hist Nat 75:307–325

    Google Scholar 

  • Bary BM (1960) Notes on ecology, distribution, and systematics of Pelagic Tunicata from New Zealand. Pac Sci 14(2):101–121

    Google Scholar 

  • Bassham S, Postlethwait J (2000) Brachyury (T) expression in embryos of a larvacean urochordate, Oikopleura dioica, and the ancestral role of T. Dev Biol 220:322–332

    Article  CAS  PubMed  Google Scholar 

  • Bedo AW, Acuña JL, Robins D, Harris RP (1993) Grazing in the micron and the sub-micron particle size range: the case of Oikopleura dioica (Appendicularia). Bull Mar Sci 52:2–14

    Google Scholar 

  • Berna L, Alvarez-Valin F (2014) Evolutionary genomics of fast evolving tunicates. Genome Biol Evol 6:1724–1738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berna L, D’onofrio G, Alvarez-Valin F (2012) Peculiar patterns of amino acid substitution and conservation in the fast evolving tunicate Oikopleura dioica. Mol Phylogenet Evol 62:708–717

    Article  CAS  PubMed  Google Scholar 

  • Blumenthal T (2004) Operons in eukaryotes. Brief Funct Genomic Proteomic 3:199–211

    Article  CAS  PubMed  Google Scholar 

  • Bollner T, Holmberg K, Olsson R (1986) A rostral sensory mechanism in Oikopleura dioica (Appendicularia). Acta Zool (Stockholm) 67:235–241

    Article  Google Scholar 

  • Bone Q (1998) The biology of pelagic tunicates. Oxford University Press, New York

    Google Scholar 

  • Bone Q, Mackie GO (1975) Skin impulses and locomotion in Oikopleura (tunicata: larvacea). Biol Bull 149:267–286

    Article  CAS  PubMed  Google Scholar 

  • Bouquet JM, Spriet E, Troedsson C, Ottera H, Chourrout D, Thompson EM (2009) Culture optimization for the emergent zooplanktonic model organism Oikopleura dioica. J Plankton Res 31:359–370

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouquet JM, Troedsson C, Novac A, Reeve M, Lechtenborger AK, Massart W, Skaar KS, Aasjord A, Dupont S, Thompson EM (2018) Increased fitness of a key appendicularian zooplankton species under warmer, acidified seawater conditions. PLoS One 13:e0190625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bowles J, Schepers G, Koopman P (2000) Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227:239–255

    Article  CAS  PubMed  Google Scholar 

  • Brozovic M, Martin C, Dantec C, Dauga D, Mendez M, Simion P, Percher M, Laporte B, Scornavacca C, Di Gregorio A, Fujiwara S, Gineste M, Lowe EK, Piette J, Racioppi C, Ristoratore F, Sasakura Y, Takatori N, Brown TC, Delsuc F, Douzery E, Gissi C, Mcdougall A, Nishida H, Sawada H, Swalla BJ, Yasuo H, Lemaire P (2016) ANISEED 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic Acids Res 44:D808–D818

    Article  CAS  PubMed  Google Scholar 

  • Brozovic M, Dantec C, Dardaillon J, Dauga D, Faure E, Gineste M, Louis A, Naville M, Nitta KR, Piette J, Reeves W, Scornavacca C, Simion P, Vincentelli R, Bellec M, Aicha SB, Fagotto M, Gueroult-Bellone M, Haeussler M, Jacox E, Lowe EK, Mendez M, Roberge A, Stolfi A, Yokomori R, Brown CT, Cambillau C, Christiaen L, Delsuc F, Douzery E, Dumollard R, Kusakabe T, Nakai K, Nishida H, Satou Y, Swalla B, Veeman M, Volff JN, Lemaire P (2017) ANISEED 2017: extending the integrated ascidian database to the exploration and evolutionary comparison of genome-scale datasets. Nucleic Acids Res 46:D718–D725

    Article  PubMed Central  CAS  Google Scholar 

  • Burighel P, Brena C (2001) Gut ultrastructure of the appendicularian Oikopleura dioica (Tunicata). Invertebr Biol 120:278–293

    Article  Google Scholar 

  • Burke M, Scholl EH, Bird DM, Schaff JE, Colman SD, Crowell R, Diener S, Gordon O, Graham S, Wang X, Windham E, Wright GM, Opperman CH (2015) The plant parasite Pratylenchus coffeae carries a minimal nematode genome. Nematology 17:621

    Article  CAS  Google Scholar 

  • Calatayud S, Garcia-Risco M, Rojas NS, Espinosa-Sanchez L, Artime S, Palacios O, Cañestro C, Albalat R (2018) Metallothioneins of the urochordate Oikopleura dioica have Cys-rich tandem repeats, large size and cadmium-binding preference. Metallomics 10:1585–1594

    Article  CAS  PubMed  Google Scholar 

  • Campsteijn C, Ovrebo JI, Karlsen BO, Thompson EM (2012) Expansion of cyclin D and CDK1 paralogs in Oikopleura dioica, a chordate employing diverse cell cycle variants. Mol Biol Evol 29:487–502

    Article  CAS  PubMed  Google Scholar 

  • Cañestro C, Albalat R (2012) Transposon diversity is higher in amphioxus than in vertebrates: functional and evolutionary inferences. Brief Funct Genomics 11:131–141

    Article  PubMed  CAS  Google Scholar 

  • Cañestro C, Postlethwait JH (2007) Development of a chordate anterior-posterior axis without classical retinoic acid signaling. Dev Biol 305:522–538

    Article  PubMed  CAS  Google Scholar 

  • Cañestro C, Roncalli V (2018) Gene losses did not stop the evolution of big brains. elife 7:e41912

    Article  PubMed  PubMed Central  Google Scholar 

  • Cañestro C, Bassham S, Postlethwait JH (2003) Seeing chordate evolution through the Ciona genome sequence. Genome Biol 4:208–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Cañestro C, Bassham S, Postlethwait JH (2005) Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain. Dev Biol 285:298–315

    Article  PubMed  CAS  Google Scholar 

  • Cañestro C, Postlethwait JH, Gonzalez-Duarte R, Albalat R (2006) Is retinoic acid genetic machinery a chordate innovation? Evol Dev 8:394–406

    Article  PubMed  Google Scholar 

  • Cañestro C, Yokoi H, Postlethwait JH (2007) Evolutionary developmental biology and genomics. Nat Rev Genet 8:932–942

    Article  PubMed  CAS  Google Scholar 

  • Cañestro C, Bassham S, Postlethwait JH (2008) Evolution of the thyroid: Anterior-posterior regionalization of the Oikopleura endostyle revealed by Otx, Pax 2/5/8, and Hox1 expression. Dev Dyn 237:1490–1499

    Article  PubMed  Google Scholar 

  • Cañestro C, Albalat R, Postlethwait JH (2010) Oikopleura dioica alcohol dehydrogenase class 3 provides new insights into the evolution of retinoic acid synthesis in chordates. Zool Sci 27:128–133

    Article  CAS  Google Scholar 

  • Cañestro C, Albalat R, Irimia M, Garcia-Fernandez J (2013) Impact of gene gains, losses and duplication modes on the origin and diversification of vertebrates. Semin Cell Dev Biol 24:83–94

    Article  PubMed  Google Scholar 

  • Captanio FL, Curelovich J, Tresguerres M, Negri RM, Viñas MD, Esnal GB (2008) Seasonal cycle of appendicularians at a coastal station (38°28′S, 57°41′W) of the SW Atlantic Ocean. Bull Mar Sci 82:171–184

    Google Scholar 

  • Chalopin D, Naville M, Plard F, Galiana D, Volff JN (2015) Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol 7:567–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang ES, Neuhof M, Rubinstein ND, Diamant A, Philippe H, Huchon D, Cartwright P (2015) Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proc Natl Acad Sci USA 112:14912–14917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chavali S, Morais DA, Gough J, Babu MM (2011) Evolution of eukaryotic genome architecture: insights from the study of a rapidly evolving metazoan, Oikopleura dioica: non-adaptive forces such as elevated mutation rates may influence the evolution of genome architecture. BioEssays 33:592–601

    Article  CAS  PubMed  Google Scholar 

  • Cima F, Brena C, Burighel P (2002) Multifarious activities of gut epithelium in an appendicularian (Oikopleura dioica: Tunicata). Mar Biol 141:479–490

    Article  CAS  Google Scholar 

  • Clarke T, Bouquet JM, Fu X, Kallesoe T, Schmid M, Thompson EM (2007) Rapidly evolving lamins in a chordate, Oikopleura dioica, with unusual nuclear architecture. Gene 396:159–169

    Article  CAS  PubMed  Google Scholar 

  • Cleaver O, Krieg PA (2001) Notochord patterning of the endoderm. Dev Biol 234:1–12

    Article  CAS  PubMed  Google Scholar 

  • Coppola U, Ristoratore F, Albalat R, D’aniello S (2019) The evolutionary landscape of the Rab family in chordates. Cell Mol Life Sci. https://doi.org/10.1007/s00018-019-03103-7

  • Corbo JC, Di Gregorio A, Levine M (2001) The ascidian as a model organism in developmental and evolutionary biology. Cell 106:535–538

    Article  CAS  PubMed  Google Scholar 

  • Costello J, Stancyk SE (1983) Tidal influence upon appendicularian abundance in North Inlet estuary, South Carolina. J Plankton Res 5:263–277

    Article  Google Scholar 

  • Danks G, Campsteijn C, Parida M, Butcher S, Doddapaneni H, Fu B, Petrin R, Metpally R, Lenhard B, Wincker P, Chourrout D, Thompson EM, Manak JR (2013) OikoBase: a genomics and developmental transcriptomics resource for the urochordate Oikopleura dioica. Nucleic Acids Res 41:D845–D853

    Article  CAS  PubMed  Google Scholar 

  • Davoll P, Youngbluth M (1990) Heterotrophic activity on appendicularian (Tunicata: Appendicularia) houses in mesopelagic regions and their potential contribution to particle flux. Deep-Sea Res 37:285–294

    Article  Google Scholar 

  • Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomoso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KEM, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang H-G, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, Desantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee B-I, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-I T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167

    Article  CAS  PubMed  Google Scholar 

  • Delsman HC (1910) Beiträge zur Entwicklungsgeschichte von Oikopleura dioica. Verh Rijksinst Onderz Zee 3:1–24

    Google Scholar 

  • Delsman HC (1912) Weitere beobachtungen über die entwicklung von Oikopleura dioica. Tijdschr ned dierk Ver 12:199–206

    Google Scholar 

  • Delsuc F, Philippe H, Tsagkogeorga G, Simion P, Tilak MK, Turon X, Lopez-Legentil S, Piette J, Lemaire P, Douzery EJP (2018) A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biol 16:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng W, Henriet S, Chourrout D (2018) Prevalence of mutation-prone microhomology-mediated end joining in a chordate lacking the c-NHEJ DNA repair pathway. Curr Biol 28(3337–3341):e3334

    Google Scholar 

  • Denoeud F, Henriet S, Mungpakdee S, Aury JM, Da Silva C, Brinkmann H, Mikhaleva J, Olsen LC, Jubin C, Cañestro C, Bouquet JM, Danks G, Poulain J, Campsteijn C, Adamski M, Cross I, Yadetie F, Muffato M, Louis A, Butcher S, Tsagkogeorga G, Konrad A, Singh S, Jensen MF, Cong EH, Eikeseth-Otteraa H, Noel B, Anthouard V, Porcel BM, Kachouri-Lafond R, Nishino A, Ugolini M, Chourrout P, Nishida H, Aasland R, Huzurbazar S, Westhof E, Delsuc F, Lehrach H, Reinhardt R, Weissenbach J, Roy SW, Artiguenave F, Postlethwait JH, Manak JR, Thompson EM, Jaillon O, Du Pasquier L, Boudinot P, Liberles DA, Volff JN, Philippe H, Lenhard B, Roest Crollius H, Wincker P, Chourrout D (2010) Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330:1381–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deriano L, Roth DB (2013) Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu Rev Genet 47:433–455

    Article  CAS  PubMed  Google Scholar 

  • Duboule D (2007) The rise and fall of Hox gene clusters. Development 134:2549–2560

    Article  CAS  PubMed  Google Scholar 

  • Edvardsen RB, Lerat E, Maeland AD, Flat M, Tewari R, Jensen MF, Lehrach H, Reinhardt R, Seo HC, Chourrout D (2004) Hypervariable and highly divergent intron-exon organizations in the chordate Oikopleura dioica. J Mol Evol 59:448–457

    Article  CAS  PubMed  Google Scholar 

  • Edvardsen RB, Seo HC, Jensen MF, Mialon A, Mikhaleva J, Bjordal M, Cartry J, Reinhardt R, Weissenbach J, Wincker P, Chourrout D (2005) Remodelling of the homeobox gene complement in the tunicate Oikopleura dioica. Curr Biol 15:R12–R13

    Article  CAS  PubMed  Google Scholar 

  • Essenberg CE (1922) The seasonal distribution of the Appendicularia in the region of San Diego, California. Ecology 3:55–64

    Article  Google Scholar 

  • Fenaux R (1972) A historical survey of the appendicularians from the area covered by the IIOE. Mar Biol 16:230–235

    Article  Google Scholar 

  • Fenaux R (1976) Cycle vital d’un appendiculaire: Oikopleura dioica Fol, 1872. Ann Inst Océanogr Paris 52:89–101

    Google Scholar 

  • Fenaux R (1986) The house of Oikopleura dioica (Tunicata, Appendicularia): structure and functions. Zoomorphology 106:224–231

    Article  Google Scholar 

  • Fenaux R (1998a) Anatomy and functional morphology of the Appendicularia. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, New York

    Google Scholar 

  • Fenaux R (1998b) Life history of the Appendicularia. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, Oxford

    Google Scholar 

  • Fenaux R, Gorsky G (1985) Nouvelle technique d’élevage des appendiculaires. Rapp Comm Int Mer Médit 29:291–292

    Google Scholar 

  • Fenaux R, Bone Q, Deibel D (1998) Appendicularian distribution and zoogeography. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, Oxford

    Google Scholar 

  • Fernández D, López-Urrutia A, Fernández A, Acuña JL, Harris R (2004) Retention efficiency of 0.2 to 6 μm particles by the appendicularians Oikopleura dioica and Fritillaria borealis. Mar Ecol Prog Ser 266:89–101

    Article  Google Scholar 

  • Ferrier DE (2011) Tunicates push the limits of animal evo-devo. BMC Biol 9:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrier DEK, Sogabe S (2018) Genome biology: unconventional DNA repair in an extreme genome. Curr Biol 28:R1208–R1210

    Article  CAS  PubMed  Google Scholar 

  • Flood PR, Afzelius BA (1978) The spermatozoon of Oikopleura dioica Fol (Larvacea, Tunicata). Cell Tissue Res 191:27–37

    Article  CAS  PubMed  Google Scholar 

  • Flood PR, Deibel D (1998) The appendicularian house. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, Oxford

    Google Scholar 

  • Fol H (1872) Etudes sur les Appendiculaires du Détroit de Messine. Mem Soc Physique Hist Nat Geneve 21:445

    Google Scholar 

  • Fredriksson G, Olsson R (1981) The oral gland cells of Oikopleura dioica (Tunicata Appendicularia). Acta Zool (Stockholm) 62:195–200

    Article  Google Scholar 

  • Fredriksson G, Olsson R (1991) The subchordal cells of Oikopleura dioica and Oikopleura albicans (Appendicularia, Chrodata). Acta Zool (Stockholm) 72:251–256

    Article  Google Scholar 

  • Fredriksson G, Ofverholm T, Ericson LE (1985) Ultrastructural demonstration of iodine binding and peroxidase activity in the endostyle of Oikopleura dioica (Appendicularia). Gen Comp Endocrinol 58:319–327

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Adamski M, Thompson EM (2008) Altered miRNA repertoire in the simplified chordate, Oikopleura dioica. Mol Biol Evol 25:1067–1080

    Article  CAS  PubMed  Google Scholar 

  • Fujii S, Nishio T, Nishida H (2008) Cleavage pattern, gastrulation, and neurulation in the appendicularian, Oikopleura dioica. Dev Genes Evol 218:69–79

    Article  PubMed  Google Scholar 

  • Gabaldon T, Capella-Gutierrez S (2010) Lack of phylogenetic support for a supposed actinobacterial origin of peroxisomes. Gene 465:61–65

    Article  CAS  PubMed  Google Scholar 

  • Gabaldon T, Snel B, Van Zimmeren F, Hemrika W, Tabak H, Huynen MA (2006) Origin and evolution of the peroxisomal proteome. Biol Direct 1:8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galt CP (1972) Development of Oikopleura dioica (Urochordata: Larvacea): ontogeny of behavior and of organ systems related to construction and use of the house. PhD, University of Washington, Seattle

    Google Scholar 

  • Galt C (1978) Bioluminescence: dual mechanism in a planktonic tunicate produces brilliant surface display. Science 200:70–72

    Article  CAS  PubMed  Google Scholar 

  • Galt CP, Fenaux R (1990) Urochordata larvacea. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. Oxford and IBH, New Delhi

    Google Scholar 

  • Ganot P, Kallesoe T, Reinhardt R, Chourrout D, Thompson EM (2004) Spliced-leader RNA trans splicing in a chordate, Oikopleura dioica, with a compact genome. Mol Cell Biol 24:7795–7805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganot P, Bouquet JM, Kallesoe T, Thompson EM (2007) The Oikopleura coenocyst, a unique chordate germ cell permitting rapid, extensive modulation of oocyte production. Dev Biol 302:591–600

    Article  CAS  PubMed  Google Scholar 

  • Gaughan D, Potter IC (1994) Relative abundance and seasonal changes in the macrozooplankton of the lower estuary in South-Western Australia. Rec West Aust Mus 16:461–474

    Google Scholar 

  • Georges D, Holmberg K, Olsson R (1988) The ventral midbrain cells in Oikopleura dioica (Appendicularia). Acta Embryol Morphol Exp 9:39–47

    Google Scholar 

  • Goldschmidt R (1903) Notiz über die Entwickekung der Appendicularien-Biologisches Centralblatt, Band

    Google Scholar 

  • Goldstone JV, Hamdoun A, Cole BJ, Howard-Ashby M, Nebert DW, Scally M, Dean M, Epel D, Hahn ME, Stegeman JJ (2006) The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Dev Biol 300:366–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstone JV, Mcarthur AG, Kubota A, Zanette J, Parente T, Jonsson ME, Nelson DR, Stegeman JJ (2010) Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish. BMC Genomics 11:643

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gorsky G, Fenaux R (1998) The role of Appendicularia in marine food webs. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, Oxford

    Google Scholar 

  • Gorsky G, Fisher N, Fowler S (1984) Biogenic debris from the pelagic tunicate Oikopleura dioica and its role in the vertical transport of a transuranium element. Est Coast Shelf Sci 18:13–23

    Article  Google Scholar 

  • Handberg-Thorsager M, Gutierrez-Mazariegos J, Arold ST, Kumar Nadendla E, Bertucci PY, Germain P, Tomancak P, Pierzchalski K, Jones JW, Albalat R, Kane MA, Bourguet W, Laudet V, Arendt D, Schubert M (2018) The ancestral retinoic acid receptor was a low-affinity sensor triggering neuronal differentiation. Sci Adv 4:eaao1261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heenan P, Zondag L, Wilson MJ (2016) Evolution of the Sox gene family within the chordate phylum. Gene 575:385–392

    Article  CAS  PubMed  Google Scholar 

  • Hertel J, Lindemeyer M, Missal K, Fried C, Tanzer A, Flamm C, Hofacker IL, Stadler PF, Students of Bioinformatics Computer Labs A (2006) The expansion of the metazoan microRNA repertoire. BMC Genomics 7:25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holland LZ (2016) Tunicates. Curr Biol 26:R146–R152

    Article  CAS  PubMed  Google Scholar 

  • Holland LZ, Gibson-Brown J (2003) The Ciona intestinalis genome: when the constraints are off. BioEssays 25:529–532

    Article  CAS  PubMed  Google Scholar 

  • Holland L, Gorsky G, Fenaux R (1988) Fertilization in Oikopleura dioica (Tunicata, Appendicularia): acrosome reaction, cortical reaction and sperm-egg fusion. Zoomorphology 108:229–243

    Article  Google Scholar 

  • Holland PW, Booth HA, Bruford EA (2007) Classification and nomenclature of all human homeobox genes. BMC Biol 5:47

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holmberg K (1982) The ciliated brain duct of Oikopleura dioica (Tunicata, Appendicularia). Acta Zool 63:101–109

    Article  Google Scholar 

  • Holmberg K (1984) A transmission electron microscopic investigation of the sensory vesicle in the brain of Oikopleura dioica (Appendicularia). Zoomorphology 104:298–303

    Article  Google Scholar 

  • Hopcroft RR, Roff JC (1995) Zooplankton growth rates: extraordinary production by the larvacean Oikopleura dioica in tropical waters. J Plankton Res 17:205–220

    Article  Google Scholar 

  • Hopcroft RR, Roff JC, Bouman HA (1998) Zooplankton growth rates: the larvaceans Appendicularia, Fritillaria and Oikopleura in tropical waters. J Plankton Res 20:539–555

    Article  Google Scholar 

  • Hosp J, Sagane Y, Danks G, Thompson EM (2012) The evolving proteome of a complex extracellular matrix, the Oikopleura house. PLoS One 7:e40172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes AL, Friedman R (2005) Loss of ancestral genes in the genomic evolution of Ciona intestinalis. Evol Dev 7:196–200

    Article  CAS  PubMed  Google Scholar 

  • Hwan Lee J, Chae J, Kim W-R, Won Jung S, Man Kim J (2001) Seasonal variation of phytoplankton and zooplankton communities in the Coastal Waters off Tongyeong in Korea. Ocean Polar Res 23:245–253

    Google Scholar 

  • Inoue J, Satoh N (2018) Deuterostome genomics: lineage-specific protein expansions that enabled chordate muscle evolution. Mol Biol Evol 35:914–924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irimia M, Tena JJ, Alexis MS, Fernandez-Minan A, Maeso I, Bogdanovic O, De La Calle-Mustienes E, Roy SW, Gomez-Skarmeta JL, Fraser HB (2012) Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res 22:2356–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacob F (1977) Evolution and tinkering. Science 196:1161–1166

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Ohshima C, Hirose E, Nishikawa J, Itoh T (2001) Cellulose in the house of the appendicularian Oikopleura rufescens. Protoplasma 216:71–74

    Article  CAS  PubMed  Google Scholar 

  • King KR, Hollibaugh JT, Azam F (1980) Predator-prey interactions between the larvacean Oikopleura dioica and bacterioplankton in enclosed water columns. Mar Biol 56:49–57

    Article  Google Scholar 

  • Kishi K, Onuma TA, Nishida H (2014) Long-distance cell migration during larval development in the appendicularian, Oikopleura dioica. Dev Biol 395:299–306

    Article  CAS  PubMed  Google Scholar 

  • Kishi K, Hayashi M, Onuma TA, Nishida H (2017) Patterning and morphogenesis of the intricate but stereotyped oikoplastic epidermis of the appendicularian, Oikopleura dioica. Dev Biol 428:245–257

    Article  CAS  PubMed  Google Scholar 

  • Kmita M, Duboule D (2003) Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331–333

    Article  CAS  PubMed  Google Scholar 

  • Kocot KM, Tassia MG, Halanych KM, Swalla BJ (2018) Phylogenomics offers resolution of major tunicate relationships. Mol Phylogenet Evol 121:166–173

    Article  PubMed  Google Scholar 

  • Kugler JE, Kerner P, Bouquet JM, Jiang D, Di Gregorio A (2011) Evolutionary changes in the notochord genetic toolkit: a comparative analysis of notochord genes in the ascidian Ciona and the larvacean Oikopleura. BMC Evol Biol 11:21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusakabe T, Araki I, Satoh N, Jeffery WR (1997) Evolution of chordate actin genes: evidence from genomic organization and amino acid sequences. J Mol Evol 44:289–298

    Article  CAS  PubMed  Google Scholar 

  • Larson RJ (1987) Daily ration and predation by medusae and ctenophores in Saanich Inlet, B.C., Canada. Neth J Sea Res 21:35–44

    Article  Google Scholar 

  • Last JM (1972) Egg development, fecundity and growth of Oikopleura Dioica Fol in the North Sea. ICES J Mar Sci 34:232–237

    Article  Google Scholar 

  • Lohmann H (1933) Erste Klasse der Tunicaten: Appendiculariae. In: Kükenthal W, Krumbach T (eds) Handbuch der Zoologie. Walter De Gruyter, Berlin

    Google Scholar 

  • Lopez-Urrutia A, Acuña JL (1999) Gut throughput dynamics in the appendicularian Oikopleura dioica. Mar Ecol Prog Ser 191:195–205

    Article  Google Scholar 

  • Martinucci G, Brena C, Cima F, Burighel P (2005) Synchronous spermatogenesis in appendicularians. In: Gorsky G, Youngbluth M, Deibel D (eds) Response of marine ecosystems to global changes: ecological impact of appendicularians. Éditions des Archives Contempoaines, Paris

    Google Scholar 

  • Martí-Solans J, Ferrández-Roldán A, Godoy-Marín H, Badia-Ramentol J, Torres-Aguila NP, Rodríguez-Marí A, Bouquet JM, Chourrout D, Thompson EM, Albalat R, Cañestro C (2015) Oikopleura dioica culturing made easy: a low-cost facility for an emerging animal model in EvoDevo. Genesis 53:183–193

    Article  PubMed  Google Scholar 

  • Martí-Solans J, Belyaeva OV, Torres-Aguila NP, Kedishvili NY, Albalat R, Cañestro C (2016) Coelimination and survival in gene network evolution: dismantling the RA-signaling in a chordate. Mol Biol Evol 33:2401–2416

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Menéndez M, Biancalana F, Berasategui A, Fernández Severini MD, Hoffmeyer MS, Esteves JL (2011) Mesozooplankton composition and spatial distribution, Nuevo Gulf, Patagonia, Argentina. Check List 7:101–107

    Article  Google Scholar 

  • Mikhailov KV, Slyusarev GS, Nikitin MA, Logacheva MD, Penin AA, Aleoshin VV, Panchin YV (2016) The genome of Intoshia linei affirms orthonectids as highly simplified spiralians. Curr Biol 26:1768–1774

    Article  CAS  PubMed  Google Scholar 

  • Mikhaleva Y, Kreneisz O, Olsen LC, Glover JC, Chourrout D (2015) Modification of the larval swimming behavior in Oikopleura dioica, a chordate with a miniaturized central nervous system by dsRNA injection into fertilized eggs. J Exp Zool B Mol Dev Evol 324:114–127

    Article  CAS  Google Scholar 

  • Mikhaleva Y, Skinnes R, Sumic S, Thompson EM, Chourrout D (2018) Development of the house secreting epithelium, a major innovation of tunicate larvaceans, involves multiple homeodomain transcription factors. Dev Biol 443:117–126

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Suzuki K, Suzuki S, Hiromi J (1997) Production of Oikopleura dioica (Appendicularia) following a picoplankton ‘bloom’ in a eutrophic coastal area. J Plankton Res 19:113–124

    Article  Google Scholar 

  • Navratilova P, Danks GB, Long A, Butcher S, Manak JR, Thompson EM (2017) Sex-specific chromatin landscapes in an ultra-compact chordate genome. Epigenetics Chromatin 10:3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nelson DR, Goldstone JV, Stegeman JJ (2013) The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s. Philos Trans R Soc Lond Ser B Biol Sci 368:20120474

    Article  CAS  Google Scholar 

  • Nilsen IW, Myrnes B, Edvardsen RB, Chourrout D (2003) Urochordates carry multiple genes for goose-type lysozyme and no genes for chicken- or invertebrate-type lysozymes. Cell Mol Life Sci 60:2210–2218

    Article  CAS  PubMed  Google Scholar 

  • Nishida H (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III Up to the tissue restricted stage. Dev Biol 121:526–541

    Article  CAS  PubMed  Google Scholar 

  • Nishida H (2002) Patterning the marginal zone of early ascidian embryos: localized maternal mRNA and inductive interactions. BioEssays 24:613–624

    Article  CAS  PubMed  Google Scholar 

  • Nishida H (2008) Development of the appendicularian Oikopleura dioica: culture, genome, and cell lineages. Develop Growth Differ 50(Suppl 1):S239–S256

    Article  CAS  Google Scholar 

  • Nishida H, Stach T (2014) Cell lineages and fate maps in tunicates: conservation and modification. Zool Sci 31:645–652

    Article  Google Scholar 

  • Nishino A, Morisawa M (1998) Rapid oocyte growth and artificial fertilization of the Larvaceans Oikopleura dioica and Oikopleura longicauda. Zool Sci 15:723–727

    Article  Google Scholar 

  • Nishino A, Satoh N (2001) The simple tail of chordates: phylogenetic significance of appendicularians. Genesis 29:36–45

    Article  CAS  PubMed  Google Scholar 

  • Nishino A, Satou Y, Morisawa M, Satoh N (2000) Muscle actin genes and muscle cells in the appendicularian, Oikopleura longicauda: phylogenetic relationships among muscle tissues in the urochordates. J Exp Zool 288:135–150

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, New York

    Book  Google Scholar 

  • Olsson R (1963) Endostyles and endostylar secretions: a comparative histochemical study. Acta Zool (Stockholm) 44:299–329

    Article  CAS  Google Scholar 

  • Olsson R (1965a) Comparative morphology and physiology of the Oikopleura notochord. Isr J Zool 14:213–220

    CAS  PubMed  Google Scholar 

  • Olsson R (1965b) The cytology of the endostyle of Oikopleura dioica. Ann NY Acad Sci 118:1038–1051

    Article  CAS  PubMed  Google Scholar 

  • Olsson R (1975) Primitive coronet cells in the brain of Oikopleura (Appendicularia, Tunicata). Acta Zool (Stockholm) 56:155–161

    Article  Google Scholar 

  • Olsson R, Holmberg K, Lilliemark Y (1990) Fine structure of the brain and brain nerves of Oikopleura dioica (Urochordata, Appendicularia). Zool Morphol 110:1–7

    Google Scholar 

  • Omotezako T, Nishino A, Onuma TA, Nishida H (2013) RNA interference in the appendicularian Oikopleura dioica reveals the function of the Brachyury gene. Dev Genes Evol 223:261–267

    Article  CAS  PubMed  Google Scholar 

  • Omotezako T, Onuma TA, Nishida H (2015) DNA interference: DNA-induced gene silencing in the appendicularian Oikopleura dioica. Proc Biol Sci 282:20150435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Omotezako T, Matsuo M, Onuma TA, Nishida H (2017) DNA interference-mediated screening of maternal factors in the chordate Oikopleura dioica. Sci Rep 7:44226

    Article  PubMed  PubMed Central  Google Scholar 

  • Onuma TA, Isobe M, Nishida H (2017) Internal and external morphology of adults of the appendicularian, Oikopleura dioica: an SEM study. Cell Tissue Res 367:213–227

    Article  PubMed  Google Scholar 

  • Paffenhöfer G-A (1973) The cultivation of an appendicularian through numerous generations. Mar Biol 22:183–185

    Article  Google Scholar 

  • Pannunzio NR, Watanabe G, Lieber MR (2018) Nonhomologous DNA end-joining for repair of DNA double-strand breaks. J Biol Chem 293:10512–10523

    Article  CAS  PubMed  Google Scholar 

  • Patel AA, Steitz JA (2003) Splicing double: insights from the second spliceosome. Nat Rev Mol Cell Biol 4:960–970

    Article  CAS  PubMed  Google Scholar 

  • Raduan A, Blanco C, Soler E, Del Rio JG, Raga JA (1985) The seasonal distribution of the Appendicularia in the Bay of Cullera, Spain. Rapp Comm Int Mer Médit 29:293–294

    Google Scholar 

  • Robinson AJ, Kunji ER, Gross A (2012) Mitochondrial carrier homolog 2 (MTCH2): the recruitment and evolution of a mitochondrial carrier protein to a critical player in apoptosis. Exp Cell Res 318:1316–1323

    Article  CAS  PubMed  Google Scholar 

  • Robison BH, Reisenbichler KR, Sherlock RE (2005) Giant larvacean houses: rapid carbon transport to the deep sea floor. Science 308:1609–1611

    Article  CAS  PubMed  Google Scholar 

  • Sagane Y, Zech K, Bouquet JM, Schmid M, Bal U, Thompson EM (2010) Functional specialization of cellulose synthase genes of prokaryotic origin in chordate larvaceans. Development 137:1483–1492

    Article  CAS  PubMed  Google Scholar 

  • Salensky W (1903) Etudes anatomiques sur les Appendiculaires. I Oikopleura vanhoeffeni Lohmann. Mem Acad Sci St Petesbourg Ser 13:1–44

    Google Scholar 

  • Salensky W (1904) Etudes anatomiques sur les Appendiculaires. II Oikopleura refescens. Fol Mem Acad Sci St Petesbourg Ser 15:1–54

    Google Scholar 

  • Salensky W (1905) Zur Morphologie der Cardialorgane der Appendicularien. Sixième Congrès International de Zoologie, Berne. Kandiget fils. Genève, 381–383

    Google Scholar 

  • Sato R, Tanaka Y, Ishimaru T (2003) Species-specific house productivity of appendicularians. Mar Ecol Prog Ser 259:163–172

    Article  Google Scholar 

  • Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295

    Article  CAS  PubMed  Google Scholar 

  • Satoh N, Satou Y, Davidson B, Levine M (2003) Ciona intestinalis: an emerging model for whole-genome analyses. Trends Genet 19:376–381

    Article  CAS  PubMed  Google Scholar 

  • Satoh N, Tagawa K, Takahashi H (2012) How was the notochord born? Evol Dev 14:56–75

    Article  CAS  PubMed  Google Scholar 

  • Satoh N, Rokhsar D, Nishikawa T (2014) Chordate evolution and the three-phylum system. Proc Biol Sci 281:20141729

    Article  PubMed  PubMed Central  Google Scholar 

  • Schluter A, Fourcade S, Ripp R, Mandel JL, Poch O, Pujol A (2006) The evolutionary origin of peroxisomes: an ER-peroxisome connection. Mol Biol Evol 23:838–845

    Article  CAS  PubMed  Google Scholar 

  • Seo H-C, Kube M, Edvardsen RB, Jensen MF, Beck A, Spriet E, Gorsky G, Thompson EM, Lehrach H, Reinhardt R, Chourrout D (2001) Miniature genome in the marine chordate Oikopleura dioica. Science 294:2506

    Article  CAS  PubMed  Google Scholar 

  • Seo HC, Edvardsen RB, Maeland AD, Bjordal M, Jensen MF, Hansen A, Flaat M, Weissenbach J, Lehrach H, Wincker P, Reinhardt R, Chourrout D (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431:67–71

    Article  CAS  PubMed  Google Scholar 

  • Sheth N, Roca X, Hastings ML, Roeder T, Krainer AR, Sachidanandam R (2006) Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res 34:3955–3967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somorjai IML, Martí-Solans J, Diaz-Gracia M, Nishida H, Imai KS, Escriva H, Cañestro C, Albalat R (2018) Wnt evolution and function shuffling in liberal and conservative chordate genomes. Genome Biol 19:98

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soviknes AM, Glover JC (2007) Spatiotemporal patterns of neurogenesis in the appendicularian Oikopleura dioica. Dev Biol 311:264–275

    Article  PubMed  CAS  Google Scholar 

  • Soviknes AM, Glover JC (2008) Continued growth and cell proliferation into adulthood in the notochord of the appendicularian Oikopleura dioica. Biol Bull 214:17–28

    Article  PubMed  Google Scholar 

  • Soviknes AM, Chourrout D, Glover JC (2005) Development of putative GABAergic neurons in the appendicularian urochordate Oikopleura dioica. J Comp Neurol 490:12–28

    Article  CAS  PubMed  Google Scholar 

  • Soviknes AM, Chourrout D, Glover JC (2007) Development of the caudal nerve cord, motoneurons, and muscle innervation in the appendicularian urochordate Oikopleura dioica. J Comp Neurol 503:224–243

    Article  PubMed  CAS  Google Scholar 

  • Spada F, Steen H, Troedsson C, Kallesoe T, Spriet E, Mann M, Thompson EM (2001) Molecular patterning of the oikoplastic epithelium of the larvacean tunicate Oikopleura dioica. J Biol Chem 276:20624–20632

    Article  CAS  PubMed  Google Scholar 

  • Stach TG (2009) Anatomy of the trunk mesoderm in tunicates: homology considerations and phylogenetic interpretation. Zoomorphology 128:97–109

    Article  Google Scholar 

  • Stach T, Anselmi C (2015) High-precision morphology: bifocal 4D-microscopy enables the comparison of detailed cell lineages of two chordate species separated for more than 525 million years. BMC Biol 13:113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stach T, Winter J, Bouquet JM, Chourrout D, Schnabel R (2008) Embryology of a planktonic tunicate reveals traces of sessility. Proc Natl Acad Sci USA 105:7229–7234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stemple DL (2005) Structure and function of the notochord: an essential organ for chordate development. Development 132:2503–2512

    Article  CAS  PubMed  Google Scholar 

  • Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119

    Article  CAS  PubMed  Google Scholar 

  • Thompson EM, Kallesøe T, Spada F (2001) Diverse genes expressed in distinct regions of the trunk epithelium define a monolayer cellular template for construction of the oikopleurid house. Dev Biol 238:260–273

    Article  CAS  PubMed  Google Scholar 

  • Tomita M, Shiga N, Ikeda T (2003) Seasonal occurrence and vertical distribution of appendicularians in Toyama Bay, southern Japan Sea. J Plankton Res 25:579–589

    Article  Google Scholar 

  • Torres-Aguila NP, Martí-Solans J, Ferrandez-Roldan A, Almazan A, Roncalli V, D’aniello S, Romano G, Palumbo A, Albalat R, Cañestro C (2018) Diatom bloom-derived biotoxins cause aberrant development and gene expression in the appendicularian chordate Oikopleura dioica. Commun Biol 1:121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Troedsson C, Bouquet J-M, Aksnes DL, Thompson EM (2002) Resource allocation between somatic growth and reproductive output in the pelagic chordate Oikopleura dioica allows opportunistic response to nutritional variation. Mar Ecol Prog Ser 243:83–91

    Article  Google Scholar 

  • Troedsson C, Bouquet J-M, Lobon C, Novac A, Nejstgaard J, Dupont S, Bosak S, Jakobsen H, Romanova N, Pankoke L, Isla A, Dutz JR, Sazhin A, Thompson E (2013) Effects of ocean acidification, temperature and nutrient regimes on the appendicularian Oikopleura dioica: a mesocosm study. Mar Biol 160:2175–2187

    Article  CAS  Google Scholar 

  • Uren AG, O’rourke K, Aravind LA, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6:961–967

    CAS  PubMed  Google Scholar 

  • Uye S-I, Ichino S (1995) Seasonal variations in abundance, size composition, biomass and production rate of Oikopleura dioica (Fol) (Tunicata: Appendicularia) in a temperate eutrophic inlet. J Exp Mar Biol Ecol 189:1–11

    Article  Google Scholar 

  • Volff JN, Lehrach H, Reinhardt R, Chourrout D (2004) Retroelement dynamics and a novel type of chordate retrovirus-like elements in the miniature genome of the tunicate Oikopleura dioica. Mol Biol Evol 21:2022–2033

    Article  CAS  PubMed  Google Scholar 

  • Walkusz W, Storemark K, Skau T, Gannefors C, Lundberg M (2003) Zooplankton community structure; a comparison of fjords, open water and ice stations in the Svalbard area. Pol Polar Res 24:149–165

    Google Scholar 

  • Wang K, Dantec C, Lemaire P, Onuma TA, Nishida H (2017) Genome-wide survey of miRNAs and their evolutionary history in the ascidian, Halocynthia roretzi. BMC Genomics 18:314

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wegner M (2010) All purpose Sox: the many roles of Sox proteins in gene expression. Int J Biochem Cell Biol 42:381–390

    Article  CAS  PubMed  Google Scholar 

  • Weill M, Philips A, Chourrout D, Fort P (2005) The caspase family in urochordates: distinct evolutionary fates in ascidians and larvaceans. Biol Cell 97:857–866

    Article  CAS  PubMed  Google Scholar 

  • Welsch U, Storch V (1969) On the fine structure of the chorda dorsalis in lower chordata. (Dendrodoa grossularia (v. Beneden) and Oikopleura dioica Fol). Z Zellforsch Mikrosk Anat 93:547–549

    Article  CAS  PubMed  Google Scholar 

  • Yadetie F, Butcher S, Forde HE, Campsteijn C, Bouquet JM, Karlsen OA, Denoeud F, Metpally R, Thompson EM, Manak JR, Goksoyr A, Chourrout D (2012) Conservation and divergence of chemical defense system in the tunicate Oikopleura dioica revealed by genome wide response to two xenobiotics. BMC Genomics 13:55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarsky V, Tachezy J (2015) Evolutionary loss of peroxisomes-not limited to parasites. Biol Direct 10:74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

The authors thank all current and former members of the C.C. and R.A. laboratories for fruitful scientific discussions on evolution, gene loss, and Oikopleura dioica. We thank Annamaria Locascio for the Ciona robusta picture. C.C. was supported by BFU2016-80601-P grant, and R.A. was supported by BIO2015-67358-C2-1-P grant from Ministerio de Economía y Competitividad (Spain). C.C. and R.A. were also supported by grant SGR2017-1665 from Generalitat de Catalunya. A.F-R. was supported by a FPU14/02654 fellowship from Ministerio de Educación Cultura y Deporte.

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  1. Alfonso Ferrández-Roldán and Josep Martí-Solans contributed equally to this work.

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  1. Facultat de Biologia, Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Catalonia, Spain

    Alfonso Ferrández-Roldán, Josep Martí-Solans, Cristian Cañestro & Ricard Albalat

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  1. Alfonso Ferrández-Roldán
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  1. Institute of Zoology and Biomedical Research, Jagiellonian University, Krakow, Poland

    Waclaw Tworzydlo

  2. Institute of Zoology and Biomedical Research, Jagiellonian University, Krakow, Poland

    Szczepan M. Bilinski

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Ferrández-Roldán, A., Martí-Solans, J., Cañestro, C., Albalat, R. (2019). Oikopleura dioica: An Emergent Chordate Model to Study the Impact of Gene Loss on the Evolution of the Mechanisms of Development. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_4

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