The deuterostome ancestor

Hemichordates, the phylum of bilateral animals closest to chordates, can illuminate the evolutionary origins of various chordate traits to determine whether these were already present in a shared ancestor (the deuterostome ancestor) or were evolved within the chordate line. We find that an anteroposterior map of gene expression domains, representing 42 genes of neural patterning, is closely similar in hemichordates and chordates, though it is restricted to the neural ectoderm in chordates whereas in hemichordates, which have a diffuse nervous system, it encircles the whole body. This map allows an accurate alignment of the anterioposterior axes of members of the two groups. We propose that this map dates back at least to the deuterostome ancestor. The map of dorsoventral expression domains, organized along a Bmp-Chordin developmental axis, is also similar in the two groups in terms of many gene expression domains and for the placement of the gill slits, heart, and post-anal tail. The two groups, however, differ in two major respects along this axis. The nervous system and epidermis are not segregated into distinct territories in hemichordates, as they are in chordates, and furthermore, the mouth is on the Chordin side in hemichordates but the Bmp side in chordates. The dorsoventral dimension has undergone extensive modification in the chordate line, including centralization of the nervous system, segregation of epidermis, derivation of the notochord, perhaps from the gut midline, and relocation of the mouth. Based on the shared domain maps, speculations can be made for the remodeling of the body axis in the chordate line.     

Evolution and development of the chordates: collagen and pharyngeal cartilage

Chordates evolved a unique body plan within deuterostomes and are considered to share five morphological characters, a muscular postanal tail, a notochord, a dorsal neural tube, an endostyle, and pharyngeal gill slits. The phylum Chordata typically includes three subphyla, Cephalochordata, Vertebrata, and Tunicata, the last showing a chordate body plan only as a larva. Hemichordates, in contrast, have pharyngeal gill slits, an endostyle, and a postanal tail but appear to lack a notochord and dorsal neural tube. Because hemichordates are the sister group of echinoderms, the morphological features shared with the chordates must have been present in the deuterostome ancestor. No extant echinoderms share any of the chordate features, so presumably they have lost these structures evolutionarily. We review the development of chordate characters in hemichordates and present new data characterizing the pharyngeal gill slits and their cartilaginous gill bars. We show that hemichordate gill bars contain collagen and proteoglycans but are acellular. Hemichordates and cephalochordates, or lancelets, show strong similarities in their gill bars, suggesting that an acellular cartilage may have preceded cellular cartilage in deuterostomes. Our evidence suggests that the deuterostome ancestor was a benthic worm with gill slits and acellular gill cartilages.     

Evolution of the organizer and the chordate body plan

The discovery of the organizer by Spemann and Mangold in 1924 raised two kinds of questions: those about the means of patterning the chordate body axis and those about the mechanisms of cell determination by induction. Some researchers, stressing the second, have suggested over the years that the organizer is poorly named and doesn't really organize because inducers act permissively, because they are not unique to the organizer, and because multipotent responsive cells develop complex local differentiations under artificial conditions. Furthermore, with the discovery of meso-endoderm induction in 1969, the possibility arose that this earlier induction generates as much organization as, or more than, does the organizer itself. Evidence is summarized in this article that the organizer does fulfill its title with regard to pattern formation: it adds greatly to embryonic organization by providing information about time, place, scale, and orientation for development by nearby members of the large multipotent competence groups surrounding the organizer. Embryos having smaller or larger organizers due to experimental intervention develop defective axial organization. Without an organizer the embryo develops no body axis and none of the four chordate characters: the notochord, gill slits, dorsal hollow nerve chord, and post-anal tail. For normal axis formation, the organizer's tripartite organization is needed. Each part differs in inducers, morphogenesis, and self-differentiation. The organizer is a trait of development of all members of the chordate phylum. In comparison to hemichordates, which constitute a phylum with some similarities to chordates, the chordamesoderm part is unique to the chordate organizer (the trunk-tail organizer). Its convergent extension displaces the gastrula posterior pole from alignment with the animal-vegetal axis and generates a new anteroposterior axis orthogonal to this old one. Once it has extended to full length, its signaling modifies the dorsoventral dimension. This addition to the organizer is seen as a major event in chordate evolution, bringing body organization beyond that achieved by oocyte organization and meso-endoderm induction in other groups.     

Dorsoventral axis inversion: Enteropneust anatomy links invertebrates to chordates turned upside down

The relationships between chordates with their dorsal nerve cord and other animal groups remain unclear. The hemichordata, specifically the enteropneusta (acorn worms), have been considered a sister group to the chordata. Enteropneusts combine various chordate features (e.g. lateral gill openings, dorsal nerve cord) with features that are usually associated with gastroneuralian invertebrates (e.g. dorsal heart, circumenteric nerve ring, ventral nerve cord). Here we analyse various morphological and functional characteristics that enteropneusts share with either invertebrates or chordates in the light of our recent proposal that the chordata may derive – by bodily dorsoventral inversion – from a gastroneuralian ancestor. We show that many seemingly non-chordate features of enteropneusts will align with similar features in the chordates – provided that we compare the ventral side of an enteropneust to the dorsal side of a chordate. This inversion proposes several interesting and new putative homologies between enteropneusts and acranian chordates, such as between their epibranchial ridge/endostyle (later thyroid gland), their postanal tails, atrial walls, and also between the chordates' dorsal notochord and the enteropneusts' posteroventral pygochord. Significantly, positional homology between notochord and pygochord is also supported by the expression domains of Brachyury orthologs in vertebrates and invertebrates: a Brachyury ortholog is active in the postero ventral mesoderm in Drosophila and in the dorsal mesoderm in chordates. In conclusion, we propose that the anatomy of enteropneusts may serve as a conceptual 'missing link' between gastroneuralian invertebrates and notoneuralian chordates. We discuss whether the enteropneust's dorsoanterior nervous centre plus their ventral trunk cord then corresponds to brain and dorsal nerve cord in the chordata.     

Early development of coelomic structures in an echinoderm larva and a similarity with coelomic structures in a chordate embryo

Early coelomic development in the abbreviated development of the sea urchin Holopneustes purpurescens is described and then used in a comparison with coelomic development in chordate embryos to support homology between a single arm of the five-armed radial body plan of an echinoderm and the single bilateral axis of a chordate. The homology depends on a positional similarity between the origin of the hydrocoele in echinoderm development and the origin of the notochord in chordate development, and a positional similarity between the respective origins of the coelomic mesoderm and chordate mesoderm in echinoderm and chordate development. The hydrocoele is homologous with the notochord and the secondary podia are homologous with the somites. The homology between a single echinoderm arm and the chordate axis becomes clear when the aboral to oral growth from the archenteron in the echinoderm larva is turned anteriorly, more in line with the anterior–posterior axis of the early zygote. A dorsoventral axis inversion in chordates is not required in the proposed homology.     

Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives

Deuterostomes are a monophyletic group of animals that include the vertebrates, invertebrate chordates, ambulacrarians and xenoturbellids. Fossil representatives from most major deuterostome groups, including some phylum-level crown groups, are found in the Lower Cambrian, suggesting that evolutionary divergence occurred in the Late Precambrian, in agreement with some molecular clock estimates. Molecular phylogenies, larval morphology and the adult heart/kidney complex all support echinoderms and hemichordates as a sister grouping (Ambulacraria). Xenoturbellids are a relatively newly discovered phylum of worm-like deuterostomes that lacks a fossil record, but molecular evidence suggests that these animals are a sister group to the Ambulacraria. Within the chordates, cephalochordates share large stretches of chromosomal synteny with the vertebrates, have a complete Hox complex and are sister group to the vertebrates based on ribosomal and mitochondrial gene evidence. In contrast, tunicates have a highly derived adult body plan and are sister group to the vertebrates based on the analyses of concatenated genomic sequences. Cephalochordates and hemichordates share gill slits and an acellular cartilage, suggesting that the ancestral deuterostome also shared these features. Gene network data suggest that the deuterostome ancestor had an anterior-posterior body axis specified by Hox and Wnt genes, a dorsoventral axis specified by a BMP/chordin gradient, and was bilaterally symmetrical with left-right asymmetry determined by expression of nodal.     

Anteroposterior patterning in hemichordates and the origins of the chordate nervous system

The chordate central nervous system has been hypothesized to originate from either a dorsal centralized, or a ventral centralized, or a noncentralized nervous system of a deuterostome ancestor. In an effort to resolve these issues, we examined the hemichordate Saccoglossus kowalevskii and studied the expression of orthologs of genes that are involved in patterning the chordate central nervous system. All 22 orthologs studied are expressed in the ectoderm in an anteroposterior arrangement nearly identical to that found in chordates. Domain topography is conserved between hemichordates and chordates despite the fact that hemichordates have a diffuse nerve net, whereas chordates have a centralized system. We propose that the deuterostome ancestor may have had a diffuse nervous system, which was later centralized during the evolution of the chordate lineage.     

On a possible evolutionary link of the stomochord of hemichordates to pharyngeal organs of chordates

As a group closely related to chordates, hemichordate acorn worms are in a key phylogenic position for addressing hypotheses of chordate origins. The stomochord of acorn worms is an anterior outgrowth of the pharynx endoderm into the proboscis. In 1886 Bateson proposed homology of this organ to the chordate notochord, crowning this animal group “hemichordates.” Although this proposal has been debated for over a century, the question still remains unresolved. Here we review recent progress related to this question. First, the developmental mode of the stomochord completely differs from that of the notochord. Second, comparison of expression profiles of genes including Brachyury, a key regulator of notochord formation in chordates, does not support the stomochord/notochord homology. Third, FoxE that is expressed in the stomochord‐forming region in acorn worm juveniles is expressed in the club‐shaped gland and in the endostyle of amphioxus, in the endostyle of ascidians, and in the thyroid gland of vertebrates. Based on these findings, together with the anterior endodermal location of the stomochord, we propose that the stomochord has evolutionary relatedness to chordate organs deriving from the anterior pharynx rather than to the notochord. genesis 52:925–934, 2014. © 2014 Wiley Periodicals, Inc.     

Retinoids and nonvertebrate chordate development

Retinoic acid (RA) is required for the differentiation and morphogenesis of chordate-specific features, such as the antero-posterior regionalization of the dorsal hollow nerve cord and neural crest cells. RA receptors (RARs) have been reported exclusively in chordates, suggesting that the acquisition of the RAR gene was important for chordate evolution. A scenario is presented here for the establishment of an RAR-mediated developmental regulatory system during the course of chordate evolution. In the common chordate ancestor, RAR came to control the spatial expression pattern of Hox genes in the ectoderm and endoderm along the antero-posterior axis. In these germ layers, RA was required for the differentiation of epidermal sensory neurons and the morphogenesis of pharyngeal gill slits, respectively. As the diffuse epidermal nerve net in the chordate ancestor became centralized to form the dorsal nerve cord, the epidermal Hox expression pattern was carried into the central nervous system. Because the Hox code here came to specify neuronal identity along the antero-posterior axis, RA became inextricably linked to the antero-posterior patterning of the chordate central nervous system.     

An aboral-dorsalization hypothesis for chordate origin

Chordates originated from a common ancestor(s) shared with two other deuterostome groups, echinoderms and hemichordates, by creating a novel type of tadpole-like larva, which was characterized by a dorsal hollow neural tube and notochord. Recent molecular phylogeny supports the notion that echinoderms and hemichordates form a clade named the Ambulacraria and that, among the chordates, cephalochordates are more basal than urochordates and vertebrates. An aboral-dorsalization hypothesis is proposed to explain how the tadpole-type larva evolved. Embryological comparison of cephalochordates with nonchordate deuterostomes suggests that, because of limited space on the oral side of the ancestral embryo, morphogenesis to form the neural tube and notochord occurred on the aboral side of the embryo. Namely, the dorsalization of the aboral side of the ancestral embryo may have been a key developmental event that led to the formation of the basic chordate body plan.     

Relationships Between Invertebrate Phyla Based on Functional-Mechanical Analysis of the Hydrostatic Skeleton

SYNOPSIS. The phylogeny of the major groups of deuterostomecoelomates—the chordates,hemichordates and echinoderms—isdiscussed based on a mechanical-functional analysis of the hydrostaticskeleton and associated structures. The basic approach is tofirst establish transformation series of individual featuresand of functional complexes of features and secondto determinetheir "Lesrichtung" by showing the direction of increased economy(i.e., better adaptation) with respect to environmental factors.It is argued that a metameric coelom is primitive with respectto an oligomeric one and that the ancestral form of the deuterostomecoelomates is a metameric, coelomate worm-like animal with acomplex set of circular, transverse andlongitudinal body muscles.The coelom plus the complex body musculature formed the hydrostaticskeleton.The sequence of structural modifications leading to chordatesis: (a) appearance of the notochord; (b) specialization of thedorsal longitudinal muscles with a reduction and disappearanceof the transverse and circular muscles; (c) simultaneous appearanceof the dorsal hollow nerve cord; (d) development of a postanaltail; and (e) appearance and specialization of the branchialbasket with gill slits as a filter feeding apparatus. The primitivechordate would be most similar to the lancelet (Acrania). Tunicatesare advanced chordates specialized forsessile life and lostmost chordate features in the adult, but retained them in thelarvae as adaptations for active dispersal. Enteropneusts (acornworms) are another advanced group specialized for burrowingin fine sediments and that evolved the anterior proboscis asa peristaltic burrowing organ. The notochord was lost as wasthe dorsal nerve cord and segmented conditionof the coelom.A collar originated as a means to prevent discharged water fromre-entering themouth. Pterobranchs arose from enteropneustlikeforms; their major structural changes are reduction of the branchialbasket and modification of the collar into tentacles which areassociated with life in a closed tube. Finally, echinodermsarose from a pterobranch-like ancestor by specializing for sessilelife and feeding with tentacles and by final loss of the branchialbasket. Groups such as the tunicates, hemichordates and echinodermscould be eliminated as ancestral forms within the deuterostomecoelomates because the evolution of acraniates and vertebratesfrom each of these groups would involve the appearance of gillslits before the notochord and/or the evolution of a metamericcoelom from an oligomeric one, both of which are exceedinglyimprobable. Central to the methods used to establish the transformationseries of features and their direction of evolutionary change(Lesrichtung) are functional (mechanical) analysis and adaptiveinterpretation of features; hence, functional-adaptive analysesare an integral and essential part of the methodology of phylogeneticinvestigation.     

Evolutionary modification of mouth position in deuterostomes

In chordates, the oral ectoderm is positioned at the anterior neural boundary and is characterized by pituitary homeobox (Pitx) and overlapping Dlx and Six3 expressions. Recent studies have shown that the ectoderm molecular map is also conserved in hemichordates and echinoderms. However, the mouth develops in a more posterior position in these animals, in a domain characterized by Nkx2.1 and Goosecoid expression, in a manner similar to that observed in protostomes. Furthermore, BMP signaling antagonizes mouth development in echinoderms and hemichordates, but seems to promote oral ectoderm specification in chordates. Conversely, Nodal signaling appears to be required for oral ectoderm specification in sea urchins but not in chordates. The Nodal/BMP antagonism at work during ectoderm patterning thus seems to constitute a conserved feature in deuterostomes, and mouth relocation may have been accompanied by a change in the influence of BMP/Nodal signals on oral ectoderm specification. We suggest that the mouth primordium was located at the anterior neural boundary, in early chordate evolution. In extant chordate embryos, subsequent mouth positioning differ between urochordates and vertebrates, presumably as a consequence of surrounding tissues remodelling. We illustrate these morphogenetic movements by means of morphological data obtained by the confocal imaging of ascidian tailbud embryos, and provide a table for determining the tailbud stages of this model organism.     

Ontogeny of the collar cord: Neurulation in the hemichordate Saccoglossus kowalevskii

The chordate body plan is characterized by a central notochord, a pharynx perforated by gill pores, and a dorsal central nervous system. Despite progress in recent years, the evolutionary origin of each of theses characters remains controversial. In the case of the nervous system, two contradictory hypotheses exist. In the first, the chordate nervous system is derived directly from a diffuse nerve net; whereas, the second proposes that a centralized nervous system is found in hemichordates and, therefore, predates chordate evolution. Here, we document the ontogeny of the collar cord of the enteropneust Saccoglossus kowalevskii using transmission electron microscopy and 3D‐reconstruction based on completely serially sectioned stages. We demonstrate that the collar cord develops from a middorsal neural plate that is closed in a posterior to anterior direction. Transversely oriented ependymal cells possessing myofilaments mediate this morphogenetic process and surround the remnants of the neural canal in juveniles. A mid‐dorsal glandular complex is present in the collar. The collar cord in juveniles is clearly separated into a dorsal saddle‐like region of somata and a ventral neuropil. We characterize two cell types in the somata region, giant neurons and ependymal cells. Giant neurons connect via a peculiar cell junction that seems to function in intercellular communication. Synaptic junctions containing different vesicle types are present in the neuropil. These findings support the hypotheses that the collar cord constitutes a centralized element of the nervous system and that the morphogenetic process in the ontogeny of the collar cord is homologous to neurulation in chordates. Moreover, we suggest that these similarities are indicative of a close phylogenetic relationship between enteropneusts and chordates. J. Morphol., 2010. ©2010 Wiley‐Liss, Inc.     

Development and evolution of chordate cartilage

Deuterostomes are a monophyletic group of animals containing vertebrates, lancelets, tunicates, hemichordates, echinoderms, and xenoturbellids. Four out of these six extant groups-vertebrates, lancelets, tunicates, and hemichordates-have pharyngeal gill slits. All groups of deuterostome animals that have pharyngeal gill slits also have a pharyngeal skeleton supporting the pharyngeal openings, except tunicates. We previously found that pharyngeal cartilage in hemichordates and cephalochordates contains a fibrillar collagen protein similar to vertebrate type II collagen, but unlike vertebrate cartilage, the invertebrate deuterostome cartilages are acellular. We found SoxE and fibrillar collagen expression in the pharyngeal endodermal cells adjacent to where the cartilages form. These same endodermal epithelial cells also express Pax1/9, a marker of pharyngeal endoderm in vertebrates, lancelets, tunicates, and hemichordates. In situ experiments with a cephalochordate fibrillar collagen also showed expression in pharyngeal endoderm, as well as the ectoderm and the mesodermal coelomic pouches lining the gill bars. These results indicate that the pharyngeal endodermal cells are responsible for secretion of the cartilage in hemichordates, whereas in lancelets, all the pharyngeal cells surrounding the gill bars, ectodermal, endodermal, and mesodermal may be responsible for cartilage formation. We propose that endoderm secretion was primarily the ancestral mode of making pharyngeal cartilages in deuterostomes. Later the evolutionary origin of neural crest allowed co-option of the gene network for the secretion of pharyngeal cartilage matrix in the new migratory neural crest cell populations found in vertebrates.