Which taxa are protostomes

The importance of educating students and the faculty who teach invertebrate zoology cannot be overlooked. One problem is finding drawings and photographs of the lesser-known taxa for educational use. This makes it much easier for students to learn about them, and many of these new ideas are presented in current introductory biology texts e. The term Polychaeta may no longer be valid because Polychaeta is likely a synonym for Annelida see the paper by Halanych et al. Clearly, many taxon names are currently in flux, and the use of the conventional taxonomic levels of absolute hierarchy such as Phylum, Class, Order and Family is inconsistent and troublesome.

With all the changes and new ideas in phylogeny, new molecular tools, and with the continued discovery of new taxa for example, Reinhardt Kristensen introduced a new group of animals, the micrognathozoans, at this symposium that were discovered in a freshwater spring in Greenland , interest appears strong in continuing symposia on this topic at approximately five year intervals, perhaps rotating different taxa at different meetings.

This symposium was organized in response to requests and inquiries from a number of people at the SICB symposium on Metazoan evolution McHugh and Halanych, The symposium has a history going back to when Robert Higgins organized a refresher course on the lesser-known invertebrates at a joint meeting of the American Institute of Biological Sciences and the American Microscopical Society AMS that took place in New Orleans in , and most recently in at a joint meeting of the American Society of Zoologists and the AMS in San Antonio that was also organized by Higgins.

He has been instrumental in promoting the study of lesser-known taxa over the years. Higgins had a long career at the Smithsonian Institution, was very active in the American Society of Zoologists now SICB and played a major role in the discovery of the phylum Loricifera. Despite being retired, Bob Higgins was invited to speak at this symposium, and although he was unable to attend, he coauthored a contribution with Birger Neuhaus in these proceedings on kinorhynchs. My professional introduction to invertebrates occurred in during an ecology course taught by Robert W.

Pennak at the University of Colorado, Boulder. Each student had to design a research project. During this time, I was working in the university's cryptogamic botany lab—processing mosses and lichens for the museum at 35 cents an hour.

I asked Dr. Pennak for some ideas for a project and he told me to look at the washings from the mosses and lichens—he assured me that if done carefully, I would find some very interesting invertebrates occupying this habitat. Sure enough, I found tardigrades, thousands of tardigrades, along with bdelloid rotifers, nematodes, water mites, chironomid larvae, and a few others long forgotten. The next year, I enrolled in Pennak's two-semester course in Invertebrate Zoology.

I was now a junior at the university and by the end of that year I decided to study tardigrades as a thesis subject for my Master's degree. Pennak was very pleased and went on to tell me that there were numerous major taxa that were not as uncommon as were scientists interested in studying them.

And that I should study tardigrades. And so I did. I was awarded a James B. Duke Fellowship at Duke University in the fall of I had planned on working on marine tardigrades and possibly tardigrade embryology, but along the way, thanks to an NSF Summer Fellowship at Friday Harbor Laboratories, I found kinorhynchs, thousands of kinorynchs, and decided that since even fewer people had studied them, they would be a good addition to my academic interests.

And now to connect all of this to today's symposium. At Duke University, my doctoral advisor, C. It turned out to be every bit as interesting as he predicted.

I was assigned the Kinorhyncha, Tardigrada and Priapulida as topics to present. Over the next fifteen years or so I remained focused on the above groups. Several interesting anecdotal stories connect me historically with the discoveries of Tubiluchus and Macabbeus in the s, both aberrant priapulids. Both genera qualified for inclusion as meiofauna and their obvious relationship with the Kinorhyncha suggested that they would be interesting to add to my repetoire.

In May of , I saw the first species an adult of what was to become the phylum Loricifera about ten years later. The following year Reinhardt Kristensen also found a representative a larva and once we got our act in order, Dr. Kristensen published the discovery. The loriciferan I saw in , Pliciloricus enigmaticus , was the first of these wild predictions come true. I was asked to put it all together. At the time, most courses covered about twelve phyla adequately and simply mentioned or ignored the remaining ones thereby giving the student the impression that these were either rare, difficult to find, difficult to work with, or that no experts were available as mentors.

There may have been others, but I no longer have the information in my personal files, just some names and whatever in my little black book for that year. The morning session had several empty seats. But by afternoon, word had gotten around and the place was overflowing. I was told that I should repeat this type of presentation every so often. Another success. The highlight of the event was the presentation on then, the newest phylum in the animal kingdom, the Loricifera, by my post-doctoral student, Reinhardt Kristensen.

I remember only a few of the colleagues who made presentations, among them: William Hummon Gastrotricha , Bradford Calloway Priapulida , and me Kinorhyncha. A few years later, , I told myself it was time to retire. And so I did … or so I thought I did.

Table 1. Notes on terminology used in metazoan phylogeny. Photo courtesy of Michael S. Examples of conflicting trees depicting the phylogeny of the bilateral Metazoa.

The main differences are in the relative locations of arthropods, annelids, brachiopods, and phoronids shown in bold in both trees. In more traditional trees, the lophophorates ectoprocts, phoronids, brachiopods are a monophyletic group at the base of the deuterostomes while Nielsen places the ectoprocts within the protostomes as the sister group to the ectoprocts, leaving the brachiopods and phoronids as basal deuterostomes.

Cycloneuralia is used by Nielsen to include gastrotrichs while others exclude gastrotrichs Ehlers et al. These differences are highlighted by dashed lines in the tree. See Table 1 for additional explanation.

Names in parentheses are alternate names for the preceding taxon. Platyzoa is not completely supported by molecular analyses so is shown with dashed lines see text for details. See Dougherty et al. Photo courtesy of Robert Higgins. I thank all of the speakers and the audience for the excellent job they did in making the symposium a success. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Adoutte , A. Balavoine, N. Lartillot, O. Lespinet, B. Prud'homme, and R. The new animal phylogeny: Reliability and implications.

A , 97 Aguinaldo , A. Turbeville, L. Linford, M. Rivera, J. Garey, R. Raff, and J. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature , Austen , M. Lambshead, P. Hutchings, G. Boucher, P. Snelgrove, C. Heip, G. King, I. Koike, and C. Biodiversity links above and below the marine sediment-water interface that may influence community stability. Cons , 11 Multicellular animals, Vol. A new approach to the phylogenetic order of nature.

Springer-Verlag, Berlin. The phylogenetic system of the Metazoa. Campbell , N. Biology, 6th ed. Benjamin Cummings, New York. Cavalier-Smith , T. A revised six-kingdom system of life. Rev , 73 Cuvier , G. Hist , 19 73 Grenier, T. Andreeva, C. Cook, A. Adoutte, M. Akam, S. Carroll, and G. Hox genes in brachiopods and priapulids and protostome evolution. Dougherty , E. Brown, E. Hanson, and W. The Lower Metazoa, comparative biology and phylogeny. University of California Press, Berkeley.

Dubilier , N. The eucoelomates are blue, pseudocoelomates are red, and the acoelomates are green. Note that only in Figures 1 and 4 do the Platyhelminthes emerge as primitive groups. The protostomes as separated by Nielsen This also sets apart the Cycloneuarlia as a clade. The cladogram further sets apart a larger clade that includes the Articulata of Brusca and Brusca and the Mollusca-Sipuncula clade as a coherent group called the Schizocoela.

This is a cladogram that summarizes current molecular phylogenetics in the protostomes. It is a generalized figure from Tudge In this system, the protostomes are divided into two large groups: the Ecdysozoa and the Lophotrochozoa. Figure 1. The protostomes as separated by Brusca and Brusca This includes two large clusters: the Cycloneuralia and the Articulata along with several independent clades. The above-described interface is formed primarily by the rostral-most somite and caudal-most part of the pharynx Fig.

Thus, the hypoglossal nerve, a trunk component, circumvents the pharyngeal arches by passing along the ventral curve of the interface, and the proximal part of the vagus nerve, a head component, passes along the dorsal curve to circumvent the trunk environment Fig. This curious morphological pattern reflects the vertebrate-specific plan of morphogenetic logics, showing unique sets of structures found only in vertebrates.

Around the abovementioned interface, vertebrate-specific structures appear, including the so-called neck circumpharyngeal muscles and the nerves to innervate these muscles [ , , , ]. From the ventral part of the rostral somite-derived muscle plates, migrating muscle precursors are derived to migrate toward the ventral head region along the course of the hypoglossal nerve. These muscles, called the hypobranchial muscles, are vertebrate specific and are also found in cyclostomes, in a primitive form [ ].

As the dorsal element of the circumpharyngeal muscles, the cucullaris muscle and its nerve, the accessory nerve, are recognized as derived traits that define gnathostomes. See [ ]; also see [ ]. All these features arise in the unique embryonic environment established at the interface between the vertebrate head and trunk; this environment is not found in amphioxus Fig.

Unlike the vertebrate pharyngeal arches, the amphioxus pharyngeal wall is independently separated medially from the wall that forms the ventral surface of the body. Myotomes penetrate into this pseudo-body wall, and there is no lateral plate-like continuous sheet of mesoderm. Thus, the latter interface is truly vertebrate specific, together with the structures patterned by this interface, including the hypobranchial and cucullaris muscles and the accessory, vagus, and hypoglossal nerves.

There has been a long-standing prediction that the vertebrate head mesoderm evolved from the rostral segmented mesoderm of ancestral forms such as amphioxus [ , , ].

This originally transcendental idea was further strengthened by the discovery of epithelial coelom-like structures called head cavities in some primitive jawed vertebrates such as elasmobranchs and holocephalans [ , ]; reviewed in [ ]. However, it has also been suggested that the head cavities represent a gnathostome synapomorphy, and that their epithelial segment-like configuration has nothing to do with the hypothetical head somites: there is no substantial difference in gene expression profiles between the head cavities and non-segmented, mesenchymal head mesoderm [ , ] reviewed in [ ].

On the basis of accumulated data on the gene expression profiles in developing paraxial mesoderm, however, it has become clear that amphioxus somites are not necessarily more similar to vertebrate somites than to head mesoderm, but they share gene expression profiles known to be specific to the vertebrate head mesoderm reviewed in [ , ].

Experimentally, as well, amphioxus somites are not necessarily closer to vertebrate trunk somites than to head mesoderm; it is possible that they represent an intermediate structure [ , ].

Also see [ ] for a comparative embryological discussion. The above arguments are based on the assumption that the common ancestor of amphioxus and vertebrates possessed an anteroposteriorly elongated body, with segmental mesodermal blocks throughout the entire axis. This assumption, however, has not been substantiated, although it may be relevant to the origin and homology of segments across bilaterians. Masterman [ ] once tried to identify the origin of metameric segments in three pairs of coelomic cavities derived from gut septations in the jellyfish.

Also see [ , , ]. According to this scheme, the prototypic bilaterian mesodermal cavities have three components, the rostral-most one of which is found in the procoels in various bilaterian larvae, including the actinotrochs of phoronids, tornarian larvae of hemichordates, and auricularian larvae of echinoderms.

Vertebrate embryos also fall into this category: The premandibular cavity is often assumed to be homologous to the procoel; the head mesoderm is homologous to the mesocoel and the entire somites to the metacoel [ ]. If the early embryonic pattern of amphioxus is comparable to this scheme—especially the pattern of echinoderm larvae—then the anterior head diverticulum could represent the procoel of auricularians, and the rostral-most triangular somite would represent the mesocoel.

For other interpretations, see [ ]. This level of comparison, however, potentially refers to the pan-bilaterian coelomic developmental program, not necessarily the chordate-specific morphotype. In addition, even if mesodermal homology between vertebrates and amphioxus could be established definitively, it would not mean that their body plans are identical, because the anteroposteriorly polarized distribution of the different generative constraints that yield the somitomeric and branchiomeric patterns in vertebrates is not present in amphioxus.

From the above, it is clear that the vertebrate body plan cannot have been derived from an amphioxus-like ancestor by continuous modification. The two animal groups possess conspicuous morphotypes that are distinctly different from each other: The homology of the mouth is lost, and the topographic relationship between somites and pharynx changes, during the early evolution of chordates, giving rise to different body plans.

Chordates share only the notochord, postanal tail, and dorsal nerve chord as synapomorphies, because of the shared evolutionary history of dorsoventral inversion. However, the body plans of the three chordate lineages are as different as those found in each of the phyla among ambulacrarians, lophotrochozoans, or ecdysozoans.

Given their distinct set of morphological patterns and elements, vertebrates are more appropriately classified as an independent phylum. Metazoan taxonomy and systematics, which are basic and important issues in zoology, provide basic information to help researchers interpret the grouping of various animal species.

We believe that taxonomic interpretation must always be reexamined when new data are presented—especially new molecular data from different disciplines—as such comprehensive analyses are likely to inform more balanced decisions on classification. Here, we have discussed the possibility that Vertebrata should be recognized as an animal phylum. In light of the present subphylum rank of the Vertebrata, recognition of this possibility would facilitate future studies of the origin and evolution of vertebrates.

Gee H. Across the bridge: understanding the origin of the vertebrates. Chicago: The University of Chicago Press; Book Google Scholar. Google Scholar. Balfour FM. A treatise on comparative embryology. London: Macmillan; Yarrell WA. History of British fishes. London: John Van Voorst; Huxley TH. Observations upon the anatomy and physiology of Salpa and Pyrosoma. Philos Trans R Soc. Lamarck JB. Recherches sur les causes des principaux faits physiques.

Paris: Tome Second; Darwin C. On the origin of species. London: Murray; Haeckel E. Generelle morphologie der organismen. Germany: Verlagvon Georg Reimer; Kowalevsky A. Entwicklungsgeschichte der einfachen Ascidien. Mem Acad St Petersbourg Ser. Entwicklungsgeschichte des Amphioxus lanceolatus. Lankester ER. Notes on the embryology and classification of the animal kingdom: comprising a revision of speculation relative to the origin and significance of germ layers.

Quart J Microsc Soc. Evidence for a clade of nematodes arthropods and other moulting animals. Broad phylogenomic sampling improves resolution of the animal tree of life. Urochordates are monophyletic within the deuterostomes. Syst Biol. Zeng L, Swalla BJ. Molecular phylogeny of the protochordates: chordate evolution. Can J Zool. Chordate evolution and the three-phylum system.

Proc Roy. Satoh N. Chordate origins and evolution. NY: Academic Press; The genome of the Ctenophoe Mnemiopsis leidyi and its implications for cell type evolution. The ctenophore genome and the evolutionary origin of neural systems.

Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nielsen C. Animal evolution: interrelationships of the living phyla. New York: Oxford University Press; Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol. Massachusetts: Sinaur Associates; Phylogenic analyses unravel annelid evolution. The genome of the green anole lizard and comparative analysis with birds and mammals.

International Chicken Genome Sequence Consortium. Sequence and comparative analysis of the chicken genome provide unique perspective on vertebrate evolution. A molecular phylogeny of reptiles. Wada H, Satoh N. Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA.

Halanych KM. The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Mol Phylogenet Evol. Metchnikoff E. Uber die systematische Stellung von Balanoglossus.

Zool Anz. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida.

The amphioxus genome and the evolution of the chordate karyotype. Hemichordate genomes and deuterostome origins. Joint assembly and genetic mapping of the Atlantic horseshoe crab genome reveals ancient whole genome duplication. The house spider genome reveals an ancient whole genome duplication during arachnid evolution.

BMC Biol. Multiple large-scale gene and genome duplications during the evolution of hexapods. Archetypal organization of the amphioxus Hox gene cluster. PubMed Article Google Scholar. The amphioxus Hox cluster: deuterostome posterior flexibility and Hox Evol Devel.

The amphioxus Hox cluster: characterization, comparative genomics, and evolution. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Identical genomic organization of two hemichordate hox cluster. Unusual gene order and organization of the sea urchin hox cluster.

Genomic organization of Hox and ParaHox clusters in the echinoderm, Acanthaster planci. The draft genome of Ciona intestinalis: insight into chordate and vertebrate origins. Unusual number and genomic organization of Hox genes in the tunicate Ciona intestinalis. CAS Google Scholar. Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development.

Genome-wide network of regulatory genes for construction of a chordate embryo. Dev Biol. Duboule D. The rise and fall of Hox gene cluster.

A general scenario of Hox gene inventory variation among major sarcopterygian lineage. BMC Evol Biol. Dahn RD. Differential evolution of the 13 Atratic salmon Hox clusters. Mol Biol Evol. Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii.

Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates. Nat Ecol Evol. The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplication.

Genome Res. The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evlution. Nat Genet. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head. Kargong KV. Vertebrates Comparative anatomy, function evolution. New York: McGraw-Hill; Insights into bilaterian evolution from three spiralian genomes.

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads. Nat Eco Evol. Article Google Scholar. Budd G, Jensen S. A critical reappraisal of the fossil record of the bilaterian phyla.

Biol Rev. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl.

Raff R. The shape of life. Chicago: The university of Chicago press; Sander K. Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol.

J Exp Zool B Mol. Irie N, Sehara-Fujisawa A. The vertebrate phylotypic stage and an early bilaterian-related stage in mouse embryogenesis defined by genomic information. Domazet-Loso T, Tautz D. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Irie N, Kuratani S. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan.

Gene expression divergence recapitulates the developmental hourglass model. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell. Zalts H, Yanai I. Developmental constraints shape the evolution of the nematode mid-developmental transition. High expression of new genes in trochophore enlightening the ontogeny and evolution of trochozoans.

Sci Rep. The mid-developmental transition and the evolution of animal body plans. Pairwise comparisons across species are problematic when analyzing functional genomic data. The developmental hourglass model: a predictor of the basic body plan? Irie N. Remaining questions related to the hourglass model in vertebrate evolution.

Curr Opin Genet Dev. Embryonic lethality is not sufficient to explain hourglass-like conservation of vertebrate embryos. Suzuki D. Two-headed mutants of the lamprey, a basal vertebrate. Zool Lett. The Vertebrate Body. Philadelphia: Saunders; Jefferies RPS. The ancestry of the Vertebrates. In: British museum natural history ; Schaeffer B. Deuterostome monophyly and phylogeny.

Evol Biol. Uber Entwickelungsgeschichte der Thiere. Koenigsberg: Beobachtung und Reflektion; Noden DM. Craniofacial development: new views on old problems. Anat Rec. Origins and patterning of craniofacial mesenchymal tissues. Interactions and fates of avian craniofacial mesenchyme. Mode of reduction in the number of pharyngeal segments within the sarcopterygians.

Carroll RL. Patterns and Processes of Vertebrate Evolution. Cambridge: Cambridge Univ Press; Rosenberg A. The character concept: Adaptationalism to molecular developments. In: Wagner GP, editor. The character concept in evolutionary biology. Cambridge: Academic Press; Anthropogenie, oder, Entwickelungsgeschichte des menschen. W Engelmann: Keimes-und stammesgeschichte; Forey P, Janvier P. Agnathans and the origin of jawed vertebrates.

Janvier P. Early Vertebrates. New York: Oxford Scientific Publications; Hall BK. The neural crest in development and evolution.

New York: Springer Verlag; Mallatt J, Sullivan J. Monophyly of lampreys and hagfishes supported by nuclear DNA-coded genes. J Mol Evol. Complete mitochondrial DNA of the hagfish, Eptatretsu burgeri: the comparative analysis of mitochondrial DNA sequences strongly supports the cyclostome monophyly.