The Phylum Vertebrata: a Case for Zoological Recognition Naoki Irie1,2* , Noriyuki Satoh3 and Shigeru Kuratani4

Irie et al. Zoological Letters (2018) 4:32 https://doi.org/10.1186/s40851-018-0114-y REVIEW Open Access The phylum Vertebrata: a case for zoological recognition Naoki Irie1,2* , Noriyuki Satoh3 and Shigeru Kuratani4 Abstract The group Vertebrata is currently placed as a subphylum in the phylum Chordata, together with two other subphyla, Cephalochordata (lancelets) and Urochordata (ascidians). The past three decades, have seen extraordinary advances in zoological taxonomy and the time is now ripe for reassessing whether the subphylum position is truly appropriate for vertebrates, particularly in light of recent advances in molecular phylogeny, comparative genomics, and evolutionary developmental biology. Four lines of current research are discussed here. First, molecular phylogeny has demonstrated that Deuterostomia comprises Ambulacraria (Echinodermata and Hemichordata) and Chordata (Cephalochordata, Urochordata, and Vertebrata), each clade being recognized as a mutually comparable phylum. Second, comparative genomic studies show that vertebrates alone have experienced two rounds of whole-genome duplication, which makes the composition of their gene family unique. Third, comparative gene-expression profiling of vertebrate embryos favors an hourglass pattern of development, the most conserved stage of which is recognized as a phylotypic period characterized by the establishment of a body plan definitively associated with a phylum. This mid-embryonic conservation is supported robustly in vertebrates, but only weakly in chordates. Fourth, certain complex patterns of body plan formation (especially of the head, pharynx, and somites) are recognized throughout the vertebrates, but not in any other animal groups. For these reasons, we suggest that it is more appropriate to recognize vertebrates as an independent phylum, not as a subphylum of the phylum Chordata. Keywords: Gene family, Gene expression profile, Molecular phylogeny, Organ development, Phylum Vertebrata, Zoological classification Background classification, in the mid-to-late eighteenth century, The origin and evolution of vertebrates has long been a lancelets [4] and tunicates [5] were considered inverte- focus of zoological study [1]. Vertebrates were distin- brates and grouped with Mollusca, although Yarrell [4] guished from invertebrates as early as a few hundred noted that lancelets possess a primitive axial rod and years BC [2]. The present zoological taxonomy classifies thus show some affinity to vertebrates. In 1794, Lamarck Vertebrata as a subphylum of the phylum Chordata, to- [6] proposed the phylum Vertebrata, distinguishing them gether with two other invertebrate subphyla, Cephalo- from invertebrates (Fig. 1a). The publication of Charles chordata (lancelets) and Urochordata (ascidians). The Darwin’s book On the origin of species in 1859 [7] led to aim of this review is to discuss whether the subphylum vigorous discussion of animal evolution, including the Vertebrata is supported by data obtained from recent classification of vertebrates. In 1866, Haeckel [8], himself zoological research. a committed Darwinian, proposed a new concept for The present classifications of vertebrates was estab- phylum Vertebrata, as comprising two subphyletic lished by Balfour [3] in 1880–1881(Fig. 1a), and the sub- groups: vertebrates as Craniata (animals with heads) and phylum rank of Vertebrata has not been the subject of lancelets as Acrania (animals without heads) (Fig. 1a). critical discussion since that time. Prior to Balfour’s In1886 and 1887, Kowalevsky reported his discovery of the notochord in ascidian larvae [9] and in lancelet adults * Correspondence: [email protected] [10]. His reports impressed zoologists with the affinity of 1Department of Biological Sciences, School of Science, University of Tokyo, Tokyo 113-0033, Japan these two invertebrates with vertebrates, as all three 2Universal Biology Institute, University of Tokyo, Tokyo 113-0033, Japan groups have a notochord. Following further discussion, in Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Irie et al. Zoological Letters (2018) 4:32 Page 2 of 20 a b c Fig. 1 (See legend on next page.) Irie et al. Zoological Letters (2018) 4:32 Page 3 of 20 (See figure on previous page.) Fig. 1 Subphylum Vertebrata of the phylum Chordata. a Key reports that led to the concept of the phylum Chordata. Terms in red are of phylum rank and those in black are of subphylum rank. Those in green were recognized as invertebrates at the times indicated in the first column. b Traditional view (upper) and c our proposed view (lower) of chordate phylogeny with respect to inter-phylum relationships. The proposed phylogeny regards the Cephalochordata, the Urochordata, and the Vertebrata as separate phyla, rather than as subphyla. (modified from [17]) 1877, Lankester [11] proposed that the phylum Ver- Molecular phylogeny tebrata consisted of three subphyla: Craniata, Ceph- The introduction of molecular phylogeny and its appli- alochordata (animals with a notochord that runs cation to metazoans first occured in the 1980s. The through the entire body to the tip of trunk), and Uro- initial use of molecular phylogeny was delayed in meta- chordata (or Tunicata, animals with a notochord that zoans compared with other organisms such as prokary- is present only in the tail) (Fig. 1a). Thus, the basic otes, fungi, and plants, because metazoan phylogeny had schema for the taxonomic classification of vertebrates been discussed in terms of the distinct characteristic fea- and other notochordal taxa was fixed under Lanke- tures of each taxon, including fossil records, modes of ster’s proposed system. The following year, Balfour [3] embryogenesis, and larval and adult morphology. These altered the terminology of Vertebrata to Chordata and basic methodological approaches to metazoan classifica- Craniata to Vertebrata (Fig. 1a), further emphasizing tion were well-established and had a long history of pro- the notochord (and the dorsal nerve cord or neural viding valid insights, and thus appeared too robust to be tube); this led to the current concept of the subphy- reevaluated using other methods. However, it was soon lum Vertebrata in the phylum Chordata. recognized that molecular phylogeny is a very useful Over the past three decades, extraordinary advances method for inferring relationships between metazoan have been made in zoological classification thanks to taxa at the family and order levels. Nevertheless, there the incorporation of new methods and technologies, are a number of issues regarding the phylogenetic pos- including evolutionary developmental biology (evo-- ition of metazoan taxa at the phylum level remain, in- devo), molecular phylogeny, and comparative genom- cluding the nature of the ctenophore ancestor of all ics. Our understanding of the phylogenic position of metazoans [13, 18, 19] and the association of Xenotur- metazoan taxa or the evolutionary relationships bella with the deuterostome ancestor [20]. (The latter among bilaterian groups is now changing as a result issue is not discussed here, as we do not consider this of data obtained using these new tools. For example, animal group to fall within the scope of mainstream protostomes are now subdivided into two major deuterostome evolution.) Many molecular phylogenic re- groups—lophotrochozoans (spiralians) and ecdysozo- ports have tackled the classification or taxonomy of ans—on the basis of their molecular phylogeny (Fig. metazoans. We discuss three examples below. 1b) [12, 13]. Nevertheless, the classification of the The first example is the seminal report of two major phylum Chordata and its three sub-phylum system clades of protostomes: Lophotrochozoa (platyhelminths/ has largely remained unchallenged, although recently annelids/mollusks) and Ecdysozoa (arthropods/nema- a few researchers have come to question this tax- todes) [13]. Protostomes are the largest group of bilater- onomy. For example, Swalla et al. [14] and Zeng and ians. The traditional view of protostome phylogeny Swalla [15], on the basis of molecular phylogeny as emphasized the grade of complexity of the body plan; es- determined by 18S rDNA sequence comparison, sug- pecially the development of the body cavity or coelom gested that tunicates are monophyletic and should [21]. Protostomes were subdivided on the basis of the therefore be recognized as a phylum. Satoh et al. [16] mode of body cavity formation into acoelomates (with proposed a three-phylum system of chordates instead no distinct body cavity) such as platyhelminths; pseudo- of the three-subphylum system. Although this notion coelomates (with a poorly developed body cavity) such was viewed with interest by many zoologists, and a as nematodes; and coelomates (with a distinct body cav- growing body of research provides support for this ity) such as annelids, mollusks, and arthropods. An im- viewpoint, the proposed phyletic

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