Tunicata 4 Alberto Stolfi and Federico D
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Tunicata 4 Alberto Stolfi and Federico D. Brown Chapter vignette artwork by Brigitte Baldrian. © Brigitte Baldrian and Andreas Wanninger. A. Stolfi Department of Biology , Center for Developmental Genetics, New York University , New York , NY , USA F. D. Brown (*) EvoDevo Laboratory, Departamento de Zoologia , Instituto de Biociências, Universidade de São Paulo , São Paulo , SP , Brazil Evolutionary Developmental Biology Laboratory, Department of Biological Sciences , Universidad de los Andes , Bogotá , Colombia Centro Nacional de Acuicultura e Investigaciones Marinas (CENAIM) , Escuela Superior Politécnica del Litoral (ESPOL) , San Pedro , Santa Elena , Ecuador e-mail: [email protected] A. Wanninger (ed.), Evolutionary Developmental Biology of Invertebrates 6: Deuterostomia 135 DOI 10.1007/978-3-7091-1856-6_4, © Springer-Verlag Wien 2015 [email protected] 136 A. Stolfi and F.D. Brown Above all , perhaps , I am indebted to a decidedly the phylogenetic relationships between the three vegetative , often beautiful , and generally obscure classes and many orders and families have yet to group of marine animals , both for their intrinsic interest and for the enjoyment I have had in search- be satisfactorily settled. Appendicularia, ing for them . N. J. Berrill (1955) Thaliacea, and Ascidiacea remain broadly used in textbooks and scientifi c literature as the three classes of tunicates; however, recent molecular INTRODUCTION phylogenies have provided support for the mono- phyly of only Appendicularia and Thaliacea, but Tunicates are a group of marine fi lter-feeding not of Ascidiacea (Swalla et al. 2000 ; animals1 that have been traditionally divided into Tsagkogeorga et al. 2009 ; Wada 1998 ). A para- three classes: (1) Appendicularia, also known as phyletic Ascidiacea calls for a reevaluation of larvaceans because their free-swimming and tunicate relationships. The most up-to-date phy- pelagic adult stage resembles a larva; (2) logeny with a comprehensive taxonomic sam- Thaliacea, which includes three orders of free- pling of tunicates using 18S rRNA supports three swimming and pelagic adult forms with complex clades for the Tunicata (Fig. 4.1 ; T s a g k o g e o r g a life cycles (Salpida, Pyrosomida, and Doliolida); et al. 2009 ): (1) Appendicularia, (2) Stolidobranch and (3) Ascidiacea, colloquially referred to as sea ascidians, and (3) Aplousobranch ascidians+ squirts, 2 which is comprised of diverse sessile Phlebobranch ascidians+Thaliacea. All three solitary and colonial species and includes some groups of the latter clade show resemblance in of the most extensively studied tunicates. It was association of the gonads to the gut in concor- mainly the ascidians that served as the inspiration dance with the Enterogona classifi cation (Perrier for seminal studies in developmental biology and 1898 ). However, the precise position of the evolution conducted last century by British zool- Appendicularia and the Thaliacea remains unre- ogist and prolifi c writer N. J. Berrill, whose quote solved. Appendicularia has traditionally been appears above. considered to be at the base of the Tunicata (Wada 1998 ; Swalla et al. 2000 ), but recent molecular phylogenies place them as sister group to Evolutionary Relationships Stolidobranchia (Zeng et al. 2006 ; T s a g k o g e o r g a et al. 2009 ). On the other hand, Thaliacea gener- Although Tunicata is well established as a mono- ally groups closer to Phlebobranchia than to phyletic group and united by their indisputably Aplousobranchia using ribosomal molecular synapomorphic ability to synthesize cellulose, phylogenies (Zeng et al. 2006 ; T s a g k o g e o r g a et al. 2009 ), but the low taxonomic sampling and 1 Actually, there are specialized predatory ascidians in the a high 18S evolutionary rate of thaliaceans and Molgulidae and Octacnemidae families that do not fi lter aplousobranchs bring some uncertainty to this feed but rather swallow whole crustaceans and other grouping. In an attempt to provide an evolution- invertebrates (Tatián et al. 2011 ). ary framework of the developmental mechanisms 2 The term “sea squirt” has been adopted for these ani- in Tunicata, developmental studies of several mals, as seawater can be strongly propelled through the oral siphon upon physical perturbation. Other colloquial species of tunicates are reviewed here in a com- terms apply to certain species or genera (“sea peach” for parative manner with respect to our understand- Halocynthia aurantium, “sea grape” for Molgula spp.). ing of tunicate relationships. The literate translation for “sea squirt” is used in Spanish ( chorro de mar), Finnish ( meritupet), Swedish ( Sjöpungar), or Polish (Ż achwy); more externally descrip- Relationships to Other Chordates tive terms are also used, such as “sea bag” ( Sekkedyr in For several centuries after Linnaeus fi rst estab- Norwegian or Søpunge in Danish), “sack pipe” ( Zakpijpen lished the classifi cation system for living organ- in Dutch), or “sea sheath” or “sea vagina” ( Seescheide in isms, ascidians were grouped together based on German). Humorous, if crude, terms abound especially in Portuguese, like mija- mija (“piss-piss”), Maria Mijona adult morphological features. This group con- (“Pissing Mary”), or mijão (“big pisser”). tained a stereotypical adult body plan including [email protected] 4 Tunicata 137 Fig. 4.1 Current understanding of tunicate relationships gray ). Descriptions of the most parsimonious ancestral within the deuterostomes. Dashed lines represent possible characteristics are shown at every node representing pos- relationships in uncertain branches (see text for details). sible tunicate ancestors. Cases of multiple larval or adult Larval ( below ) and adult ( above ) forms have been ancestral forms are separated by “or”, direct development included at each node to facilitate understanding of dis- (no larva) is shown by “juvenile,” and unknown forms are tinct arguments discussed in the text of the major evolu- presented as a question mark (?) in a circle tionary transitions of extant clades and their ancestors (in (1) a U-shaped gut delimited by an incurrent and tury, tunicates were grouped together with an excurrent siphon, (2) a large branchial cavity ectoprocts and brachiopods within the mol- for fi lter feeding, and (3) the tunic, a characteris- lusks (Fig. 4.2A ) (Milne-Edwards 1843 ; Haeckel tic mantle later discovered to be made of animal 1866 ). A unifi ed Tunicata as we consider them cellulose. Already by the turn of the nineteenth today was fi rst proposed by Huxley (1851 ), who century, Jean-Baptiste de Lamarck realized that included Appendicularia in the Tunicata pro- ascidians and thaliaceans could be grouped as posed by Lamarck. Tunicata (Lamarck 1816 ). However, based Only after Kowalevsky had described the strictly on the adult morphological features of tailed larval form of ascidians (Kowalewski solitary or colonial forms, these animals remained 1866), containing a dorsal neural tube, a typical diffi cult to place in broader evolutionary animal chordate notochord, and lateral muscle cells, did groups; for example, in the mid-nineteenth cen- zoologists begin to realize that tunicates should be [email protected] 138 A. Stolfi and F.D. Brown A C B Fig. 4.2 Historic overview of the position of Tunicata twentieth century with the lophophorates (Hyman 1959 ; within the Metazoa. ( A ) View of animals relationships Zimmer and Larwood 1973; Nielsen 2002 ) basal to the through the nineteenth century (Milne-Edwards 1843 ; tunicates. ( C ) Current view using molecular phylogenies Haeckel 1866 ), highlighting the position of the Tunicata (Field et al. 1988 ; Cameron et al. 2000 ; Swalla et al. 2000 ; as a chordate due to the presence of the notochord (in red ). Winchell et al. 2002 ) ( B ) Popular view of animal relationships throughout the placed within the chordates. In the late nineteenth were placed at the base of Chordata. Because of century, zoologists such as Haeckel (1874 ) , the unique body plan of adult tunicates, it was Bateson ( 1884 , 1 8 8 6 ) , B r o o k s ( 1893 ) , W i l l e y even proposed that they be raised to phylum status ( 1894 ) , a n d G a r s t a n g (1894 ) supported Chordata (Kozloff 1990 ; C a m e r o n e t a l . 2000 ; Z e n g a n d and Hemichordata as sister phyla based on noto- Swalla 2005 ) . chord-like structures as the main synapomorphy. At the turn of the twentieth century, zoologists Within Chordata three subphyla were recognized, realized that chordates, hemichordates, and echi- Vertebrata, Cephalochordata, and Tunicata, which noderms share a common embryological trait: the Lankester (1877 ) attempted to rename as blastopore, the fi rst opening that forms in the gas- Urochordata, to highlight the evolutionary impor- trulating embryo, developed into the anus of the tance of this character within the phylum. Because adult. Thus, they were classifi ed within the super- cephalochordates shared more morphological phylum Deuterostomia (Grobben 1908 ) , o p p o s i t e features with the vertebrates, including a meta- to Protostomia, or animals whose blastopores meric muscle segmentation pattern, the tunicates developed into the mouth instead. A morphological [email protected] 4 Tunicata 139 feature that generated confusion for almost the monophyly of Deuterostomia and Ambulacraria entire twentieth century but that was relevant to the (Echinodermata + Hemichordata) and also resulted general debate of early deuterostome evolution in new and previously unexplored hypothetical rela- was the lophophore of brachiopods, ectoprocts, tionships such as the placement of Xenoturbella and phoronids (see Vol. 2, Chapters 1 0 , 1 1 , and together with acoel worms as the sister group to the 1 2 ), a crown-like feeding apparatus composed of Ambulacraria (see Vol. 1, Chapter 9 for discussion) numerous tentacles. In spite of convincing argu- or the inversion of Tunicata and Cephalochordata ments for nearly half a century that supported a positions within Chordata (Delsuc et al. 2006 ; monophyletic Lophophorata (those animals bear- Telford and Copley 2011 ). The latter proposed rela- ing a lophophore) as being part of or closely tionship for Chordata suggests that Tunicata is the related to Deuterostomia (Fig.