Acorn worms, also known as enteropneust (literally, ‘gut-breathing’) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal ‘gill’ slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.
Here, we describe the molecular patterning of chondrichthyan branchial rays (gill rays) and reveal profound developmental similarities between gill rays and vertebrate appendages. Sonic hedgehog (Shh) and fibroblast growth factor 8 (Fgf8) regulate the outgrowth and patterning of the chondrichthyan gill arch skeleton, in an interdependent manner similar to their roles in gnathostome paired appendages. Additionally, we demonstrate that paired appendages and branchial rays share other conserved developmental features, including Shh-mediated mirror-image duplications of the endoskeleton after exposure to retinoic acid, and Fgf8 expression by a pseudostratified distal epithelial ridge directing endoskeletal outgrowth. These data suggest that the skeletal patterning role of the retinoic acid/Shh/Fgf8 regulatory circuit has a deep evolutionary origin predating vertebrate paired appendages and may have functioned initially in patterning pharyngeal structures in a deuterostome ancestor of vertebrates.branchial arches ͉ development ͉ evolution ͉ limb ͉ patterning
A systematic SEM survey of tooth microstructure in (primarily) fossil taxa spanning chondrichthyan phylogeny demonstrates the presence of a superficial cap of single crystallite enameloid (SCE) on the teeth of several basal elasmobranchs, as well as on the tooth plates of Helodus (a basal holocephalan). This suggests that the epithelial-mesenchymal interactions required for the development of enameloid during odontogenesis are plesiomorphic in chondrichthyans, and most likely in toothed gnathostomes, and provides phylogenetic support for the homology of chondrichthyan and actinopterygian enameloid. Along the neoselachian stem, we see a crownward progression, possibly modulated by heterochrony, from a monolayer of SCE lacking microstructural differentiation to the complex triple-layered tooth enameloid fabric of neoselachians. Finally, the occurrence of fully-differentiated neoselachian enameloid microstructure (including compression-resistant tangle fibered enameloid and bending-resistant parallel fibered enameloid) in Chlamydoselachus anguineus, a basal Squalean with teeth that are functionally ''cladodont,'' is evidence that triple-layered enameloid microstructure was a preadaption to the cutting and gouging function of many neoselachian teeth, and thus may have played an integral role in the Mesozoic radiation of the neoselachian crown group.
Hemichordate worms possess ciliated gills on their trunk, and the homology of these structures with the pharyngeal gill slits of chordates has long been a topic of debate in the fields of evolutionary biology and comparative anatomy. Here, we show conservation of transcription factor expression between the developing pharyngeal gill pores of the hemichordate Saccoglossus kowalevskii and the pharyngeal gill slit precursors (i.e. pharyngeal endodermal outpockets) of vertebrates. Transcription factors that are expressed in the pharyngeal endoderm, ectoderm and mesenchyme of vertebrates are expressed exclusively in the pharyngeal endoderm of S. kowalevskii. The pharyngeal arches and tongue bars of S. kowalevskii lack Tbx1-expressing mesoderm, and are supported solely by an acellular collagenous endoskeleton and by compartments of the trunk coelom. Our findings suggest that hemichordate and vertebrate gills are homologous as simple endodermal outpockets from the foregut, and that much vertebrate pharyngeal complexity arose coincident with the incorporation of cranial paraxial mesoderm and neural crest-derived mesenchyme within pharyngeal arches along the chordate and vertebrate stems, respectively.
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Gegenbaur’s classical hypothesis of jaw-gill arch serial homology is widely cited, but remains unsupported by either paleontological evidence (e.g. a series of fossils reflecting the stepwise transformation of a gill arch into a jaw) or developmental genetic data (e.g. shared molecular mechanisms underlying segment identity in the mandibular, hyoid and gill arch endoskeletons). Here we show that nested expression of Dlx genes – the “Dlx code” that specifies upper and lower jaw identity in mammals and teleosts – is a primitive feature of the mandibular, hyoid and gill arches of jawed vertebrates. Using fate-mapping techniques, we demonstrate that the principal dorsal and ventral endoskeletal segments of the jaw, hyoid and gill arches of the skate Leucoraja erinacea derive from molecularly equivalent mesenchymal domains of combinatorial Dlx gene expression. Our data suggest that vertebrate jaw, hyoid and gill arch cartilages are serially homologous, and were primitively patterned dorsoventrally by a common Dlx blueprint.
Chondrichthyan fishes possess visceral skeletons that differ considerably, morphologically, from those of their sister taxon, the osteichthyans. Here, we use histological techniques and whole-mount skeletal preparations to visualize and describe the sequence of visceral skeletal condensation and chondrogenesis in a chondrichthyan, the little skate (Leucoraja erinacea). We demonstrate that visceral skeletal condensation begins rostrally, with the mandibular arch, and progresses caudally with the hyoid arch and posterior branchial arches condensing soon after. We provide a detailed account of the condensation and chondrogenesis of all major components of the L. erinacea visceral skeleton and discuss these data in the context of what is known from classical descriptions of chondrichthyan visceral skeletal development. Significant differences exist between the hypobranchial and basibranchial skeleton of L. erinacea and other chondrichthyan species, and the possible evolutionary and developmental significance of this is considered. We discuss the homology of the chondrichthyan hyoid arch and, based on patterns of mesenchymal condensation, we propose a model of condensation splitting and diversification that may account for the morphological diversification of gnathostome branchial arch derivatives. Finally, we suggest that the unique presence of certain visceral skeletal elements in chondrichthyans make oviparous chondrichthyans an ideal system for addressing questions of endoskeletal axial patterning during development.
Summary Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, while a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI-tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.
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