MBE Advance Access originally published online on November 9, 2005
Molecular Biology and Evolution 2006 23(3):541-549; doi:10.1093/molbev/msj055
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Research Article |
Evolution and Development of the Chordates: Collagen and Pharyngeal Cartilage
* Center for Developmental Biology and Biology Department, University of Washington, Seattle; and Friday Harbor Laboratories, University of Washington, Friday Harbor
E-mail: bjswalla{at}u.washington.edu.
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Abstract |
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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.
Key Words: evolution and development • chordate evolution • tunicates • cephalochordates • hemichordates • cartilage • collagen
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionSupplementary MaterialAcknowledgementsReferences |
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The unique chordate body plan evolved within the deuterostome animals sometime before the Cambrian (Valentine, Jablonski, and Erwin 1999
; Blair and Hedges 2005). Chordates traditionally include vertebrates, lancelets (cephalochordates), and tunicates, but tunicates do not exhibit a chordate body plan as adults (Zeng and Swalla 2005) (fig. 1). Hemichordates are sister group to echinoderms and both phyla are an outgroup to the rest of the chordates (Cameron, Garey, and Swalla 2000; Peterson 2004; Smith et al. 2004; Blair and Hedges 2005; Zeng and Swalla 2005) (fig. 1). Xenoturbella has been recently included in the deuterostomes as molecular evidence unites them with hemichordates and echinoderms, but their exact position within the deuterostomes is not yet clear (Bourlat et al. 2003) (fig. 1). All five chordate characteristics (postanal tail, dorsal nerve cord, notochord, endostyle, and pharyngeal gill slits) have at one time or another been suggested to have homologous structures present in hemichordates, but all these features are lacking in echinoderms and Xenoturbella, the closest relatives to hemichordates, suggesting that they were lost during their evolution (Smith et al. 2004, Zeng and Swalla 2005).
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Recent evidence suggests that hemichordates lack a notochord and a dorsal central nervous system (CNS), which are found in chordates (Lowe et al. 2003
; Gerhart, Lowe, and Kirschner 2005). These two structures are linked in chordates as the notochord induces the CNS during development (Von Straaten et al. 1988; Smith and Schoenwolf 1989; Tanabe and Jessell 1996). The notochord is a stiff rod-like structure present in chordates that provides support against the hydrostatic skeleton for propelling the animal forward when it swims (Kardong 2002). In hemichordates, an anterior diverticulum of the gut has been described as histologically similar to the chordate notochord, so has been called a stomochord (Willey 1899; Balser and Ruppert 1990). Brachyury is a T-box transcription factor that specifies notochord and is expressed in tunicate, cephalochordate, and vertebrate notochords (mesoderm) during development (Wilkinson, Bhatt, and Herrmann 1990; Yasuo and Satoh 1993, 1994; Holland et al. 1995). However, it has been shown that this gene is not expressed in the hemichordate stomochord, though it is expressed in other tissues (Peterson et al. 1999; Gerhart, Lowe, and Kirschner 2005). In sea urchins, brachyury is expressed in the secondary mesenchyme cells (mesoderm) (Harada, Yasuo, and Satoh 1995), and in Drosophila, it is expressed in the posterior gut (endoderm) (Singer et al. 1996). Thus, developmental gene expression data do not confirm the homology between the notochord and the stomochord, but it does not completely rule it out either (see Gerhart, Lowe, and Kirschner 2005).
The dorsal neural tube is a chordate characteristic at one time thought to be present in hemichordates, albeit in a more limited form, namely the collar nerve cord (Bateson 1886). Hemichordates have a diffuse nervous system composed of a middorsal nerve cord, a midventral nerve cord in the collar and trunk, as well as an epidermal nerve net throughout all body regions (Knight-Jones 1952). The dorsal nerve cord in the collar region has been hypothesized to have homology with the chordate neural tube because it is hollow and forms by rolling up into a tube during development (Morgan 1891). However, Lowe et al. (2003) recently showed that vertebrate neural-patterning genes are expressed circumferentially in the hemichordate ectoderm and, strikingly, that vertebrate forebrain genes are expressed in the proboscis ectoderm, midbrain genes in the collar ectoderm, and hindbrain genes in the trunk ectoderm. These results suggest that the deuterostome ancestor may have had an epidermal nerve net rather than a CNS, yet the anterior-posterior patterning of the ectoderm was already present (Holland 2003).
In contrast, three of the chordate characteristics are present in hemichordates, a ventral postanal tail, an endostyle, and pharyngeal gill slits. A ventral postanal tail is present in juvenile harrimaniid hemichordate worms (Bateson 1885; Burdon-Jones 1952; Cameron 2002), and it has been proposed to be homologous to the chordate postanal tail due to posterior Hox gene expression data (Lowe et al. 2003). Hemichordates have three posterior Hox genes, Hox 11/13a, 11/13b, and 11/13c, which are also found in echinoderms (Peterson 2004). Furthermore, they share specific amino acid motifs with the echinoderms (Peterson 2004), strongly supporting their sister-group relationship (Zeng and Swalla 2005). Both hemichordate Hox 11/13 and the orthologous vertebrate Hox 10-13 are expressed in the postanal tail (Lowe et al. 2003). It is interesting that a postanal tail has only been reported in species of the direct-developing Harrimaniidae (Bateson 1885; Burdon-Jones 1952; Cameron 2002), not in the Ptychoderidae (Urata and Yamaguchi 2004). These two families are paraphyletic with 18S rDNA analyses, with harrimaniids a sister group to the colonial pterobranchs (Halanych 1995; Cameron, Garey, and Swalla 2000); however, theses two families are monophyletic when a 28S rDNA (Winchell et al. 2002) or morphological (Cameron 2005) analysis is performed. A postanal tail not being present in the indirect-developing ptychoderid acorn worms means that either it was lost in ptychoderids or the direct-developing harrimaniid worms more closely resemble the chordate ancestor.
The endostyle is an iodine-binding organ present in the tunicate and cephalochordate pharynx and is considered by many researchers to be a homologous organ to the vertebrate thyroid (Sasaki et al. 2003). The hemichordate epibranchial ridge, like the chordate endostyle, is composed of specialized secretory cells (Ruppert, Cameron, and Frick 1999), and these cells bind iodine. However, iodine binding is not restricted to this region but instead occurs all throughout the pharynx (Ruppert 2005). Likewise, the hemichordate homolog of the gene NK2.1, which in chordates is expressed in the endostyle and the dorsal nervous system, was seen to be expressed in hemichordate larval neuronal structures as well as broadly in the pharyngeal endoderm, stomochord, and hindgut (Takacs, Moy, and Peterson 2002). Based on these data, it appears that the endostyle function in chordates is accomplished broadly by the pharynx in hemichordates.
The most convincing homology between hemichordates and chordates is the pharyngeal gills. The transcription factor Pax1/9 is expressed in the pharyngeal endoderm in hemichordates (Ogasawara et al. 1999; Lowe et al. 2003), tunicates (Ogasawara et al. 1999), cephalochordates (N. D. Holland and L. Z. Holland 1995), lamprey (Ogasawara et al. 2000), and gnathostomes (Neubüser, Koseki, and Balling 1995; Wallin et al. 1996; Peters et al. 1998) (fig. 2). The expression of the most anterior Hox gene, Hox1, is first seen in vertebrates in the second pharyngeal slit and the expression of Hox1 in hemichordates is seen at the level between the first and second gill slits, suggesting that the location of the gill slits along the anterior-posterior axis is also homologous (Lowe et al. 2003). Additionally, the pharyngeal skeletal elements of hemichordates and cephalochordates are strikingly similar in appearance (Hyman 1959; Schaeffer 1987). Both have been reported to contain fibrillar collagen, as seen by transmission electron microscopy (TEM) studies (Rahr 1982; Pardos and Benito 1988). Pharyngeal gills appear to function primarily for feeding and possibly for oxygen absorption, and thus in burrowing animals, cartilaginous elements may play an important structural role. All deuterostomes with gills, except for tunicates, have structural elements associated with pharyngeal gills. Tunicates lack any inner structural support but instead have a cellulose-based tunic (Rånby 1952; Matthysse et al. 2004). Phylogeny results have shown that it is likely that the ancestral deuterostome was a worm that had pharyngeal gills supported by a collagenous acellular skeleton (Cameron, Garey, and Swalla 2000; Bourlat et al. 2003; Smith et al. 2004; Zeng and Swalla 2005).
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The most abundant and studied members of the collagen family are the fibrillar collagens. Each fibrillar collagen possesses the following characteristics: a long uninterrupted triple helical collagenous domain of approximately 340 Gly-X-Y repeats, a conserved noncollagenous C-terminal domain, and an N-terminal domain with either a von Willebrand C (VWC) or thrompospondin (TSPN) domain within it (Kielty and Grant 2002
). In this article, we construct gene trees with invertebrate and vertebrate triple helical domain sequences to show that hemichordates and lancelets have at least one fibrillar collagen and that it is similar to type I and type II vertebrate collagens. We have been testing the hypothesis that hemichordates have a pharyngeal cartilage similar to vertebrates, containing collagen and proteoglycans in the matrix. Here, we show that the matrix contains at least one fibrillar collagen and probably contains proteoglycans as well, even if it is not cellular. The extracellular matrix (ECM) that comprises the gill bar skeleton in both hemichordates and cephalochordates is probably secreted by the endoderm, unlike the vertebrate pharyngeal cartilage which is neural crest derived. We hypothesize that the earliest gill cartilages were acellular, and these were gradually replaced by neural crest cells in vertebrates. Therefore, the deuterostome ancestor would have been a benthic worm with gill cartilages, a mouth, and the ability to filter feed. Cephalochordates may have lost their mouth and evolved a velum, while vertebrates lost the ability to filter feed. We next show evidence that invertebrate deuterostome cartilage is acellular, with an ECM of collagen and proteoglycans.
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Animals
Saccoglossus bromophenolosus were collected at Bay View State Park in Padilla Bay, Washington, during low tide. Worms were dug with shovels and transported back to the laboratory in 15-ml falcon tubes filled with seawater. Sites in which to dig for the worms were recognized by small circular fecal casts that the animals deposit on the surface of the mud. Branchiostoma floridae adults were purchased from Gulf Specimen Marine Lab (Panacea, Fla; http://www.gulfspecimen.org/).
Histology and Immunocytochemistry
Animals were fixed for 1 h in 4% paraformaldehyde in phosphate-buffered saline. They were then dehydrated through a 30%, 50%, 80%, and 100% ethanol series and embedded in polyester wax. Seven-micrometer sections were made on a Spencer 829 microtome and mounted on gelatin-subbed slides. The wax was removed with 100% ethanol, and slides with sections were stained with Milligan's trichrome (Presnell and Schreibman 1997) or hydrated and stained with antibodies against type II collagen (dilution 1:500) and DAPI (Sigma, St. Louis, Mo.). Photographs were taken using Cool Snap Version 1.2.0 for Macintosh and a Nikon E600 microscope. Type II collagen monoclonal antibody (ascites II-II6b3) was purchased from the Developmental Studies Hybridoma Bank (University of Iowa, Iowa City, Iowa; http://www.uiowa.edu/
dshbwww/iiii6b3.html). This monoclonal antibody is specific for vertebrate type II collagen, has a broad species specificity, and does not cross-react with vertebrate nonfibrillar collagens (Linsenmayer and Hendrix 1980).
Collagen Phylogenetic analysis
All known Homo sapiens fibrillar collagen amino acid sequences were downloaded from GenBank, and they have the following accession numbers: NP_000084.2, NP_000384.1, NP_056534.1, NP_000079.1, NP_000080.2, CAA34488.1, AAA51891.1, AAC50214.1, AAL13167.1, NP_116277.2, NP_690850.1. Invertebrate accession numbers are as follows for all known fibrillar collagens in GenBank—AAC35289.2: polychaete Alvinella pompejana; NP_999674.1, NP_999675.1: sea urchin Strongylocentrotus purpuratus; CAE53096.1: sea urchin Paracentrotus lividus; BAA75669.1, BAA75668.1: abalone Haliotis discus; and AAM77398.1: Hydra vulgaris. Tunicate fibrillar collagen sequences were downloaded from the Ciona genome Web site (http://genome.jgi-psf.org/ciona4/ciona4.home.html) and have the following gene model numbers: ci0100154301, ci0100150759, ci0100131606, ci0100144916. The mosquito Anopheles gambiae and bee Apis mellifera fibrillar collagen sequences were found via Blast on the Ensembl genome Web site (http://www.ensembl.org/Multi/blastview) and are identified by the following Ensembl novel transcript numbers: ENSANGP00000021001, ENSAPMT00000018541, ENSAPMT00000025599. The lancelet B. floridae sequence was found by Blasting the Max Planck Amphioxus gene catalogue (http://goblet.molgen.mpg.de/cgi-bin/Blast-amphioxus.cgi) with a vertebrate C-terminal fibrillar collagen domain, and it has the identifier of cluster00172.2. For all collagen sequences found via Blast, only those having a triple helical sequence in the same gene or genomic vicinity of a highly conserved noncollagenous domain (known to be present in all fibrillar collagens) were used. The hemichordate Saccoglossus kowalevskii sequence is from an expressed sequence tag (EST) clone kindly provided by John Gerhart and Marc Kirschner (Lowe at al. 2003), and its accession number is DQ233249. Amino acid sequences were trimmed to include only the major triple helix, which in complete sequences varied from 657 to 1,017 amino acids with the majority being in the 1,011–1,017 amino acid range. Each sequence in the data set is represented by a complete major helical domain except for the polychaete, hemichordate, and lancelet sequences. Because only the C-terminal ends of these sequences were available, an unknown sequence of the appropriate length was added to the N-terminus of these sequences to aid in proper alignment. These amino acid sequences were then aligned using the program ClustalX (Jeanmougin et al. 1998) and produced an alignment of 1,060 total characters.
The data set was subjected to phylogenetic analysis using PAUP* v4b10 (Swofford 1999) under the optimality criterion parsimony. To assess levels of clade support in this analysis, bootstrap support was calculated using 1,000 pseudoreplicates. Clades with values of 70 and greater were considered well supported (Hillis and Bull 1993). The data set was further analyzed using Bayesian methods (MrBayes v3.0b4) (Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003). Bayesian methods were used to compute tree topologies based on a mixed model of amino acid substitution and allowing for invariant sites and rate heterogeneity among sites (gamma parameter). The analysis was run for 1,000,000 generations, and the first 15,000 trees were discarded as burn-in after the distribution was graphed to ensure that only the trees on the plateau were included. Clades with posterior probabilities 95 and greater were considered strongly supported because they are true probabilities of clades under the assumed models (Rannala and Yang 1996).
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Results and Discussion |
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Hemichordates are tricoelomic, with an anterior proboscis, a middle neck region, and a posterior abdomen (fig. 3). The abdomen contains a number of gill slits, which are shown in figure 3A and C. In the harrimaniids, the reported range of gill slits is between 30 and 150, although the exact number will vary even within species (Smith et al. 2003
). If the worm is dissected, it is clear that there is an anterior cartilaginous proboscis skeleton and cartilaginous gill bars that support the gill pores (fig. 3B). These gill bars have been shown to stain with alcian blue (Smith et al. 2003), which stains sulfated proteoglycans. TEM studies have shown that the matrix of these gill bars appears to contain collagen fibrils (Pardos and Benito 1988), and we show here that the matrix also stains with type II collagen antibodies (fig. 4C and D).
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Milligan trichrome histology on posterior gill bars has revealed that pharyngeal endoderm cells adjacent to the gill bars appear to be secreting the matrix that makes up the gill bar matrix (fig. 4B). Hyman (1959)
also described the gill bars as a "thickening of the basement membrane of the pharyngeal epithelium." However, we cannot rule out that another population of cells could have migrated to the pharyngeal area during development and are responsible for secreting the matrix. However, developmental cell migrations have not yet been described in hemichordates or cephalochordates at these stages. In no case have any nuclei been seen within the matrix (fig. 4B–D), so it appears that the gill bars form in an acellular manner, even though Benito and Pardos (1997) show that a "wandering" nucleus from connective tissue cell can be seen on occasion within the gill bar matrix. The way that gill bars form could be similar to some types of acellular vertebrate bone formation, such as the formation of acellular vertebrae in teleost fish (Ekanayake and Hall 1987, 1988; Fleming, Keynes, and Tannahill 2004). Milligan trichrome staining on lancelet gill bars shows similar qualities to that of the hemichordate gill bars. They are acellular and adjacent to endodermally derived epithelial cells (fig. 4E and F). Also, the outer layer of these gill bars is positive for type II collagen when stained with the same monoclonal antibody (II-II6b3) as the hemichordates (fig. 4G and H).
A number of studies have attempted to determine the affinities between invertebrate fibrillar collagens and vertebrate fibrillar collagens. Some have used positive staining with vertebrate monoclonal and polyclonal antibodies (Corbetta, Bairati, and Vitellaro Zuccarello 2002; Rigo, Hartmann, and Bairati 2002; Cole and Hall 2004a, 2004b) and others phylogenetic approaches (Sicot et al. 1997; Exposito et al. 2002; Aouacheria et al. 2004). The study of Aouacheria et al. (2004) is the first to show any resolution in the evolution of invertebrate and vertebrate collagens. They accomplished this by using the major triple helical collagen domain rather than the C-terminal domain for their analysis. Their published trees appeared to have an arbitrary root placement as well as a smaller taxonomic sample, so it was not clear to what major clade of collagens the invertebrate sequences belonged. In our analysis, both parsimony and Bayesian trees show a well-supported division between the A clade and the B/C clades (fig. 5). This division is furthermore well supported in both analyses with a bootstrap value of 87 and posterior probability of 99. This division is also supported by known N-terminal domains for these two groups. All human Clade A collagen genes except for Hsa col1a2 have a VWC domain at the N-terminus, while all human clade B and C collagen genes have a TSPN domain at the N-terminus (Aouacheria et al. 2004; fig. 5).
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The majority of invertebrate sequences found to date belong to clade A based on major triple helix sequence, including abalone H. discus, polychaete A. pompejana, urchins P. lividus and S. purpuratus, lancelet B. floridae, hemichordate S. kowalevskii, and some of the sequences from bee A. mellifera and tunicate C. intestinalis. These findings are additionally corroborated by the fact that Ciona759, Urchin2, and Urchin5 have N-terminal VWC domains (Aouacheria et al. 2004
). Also, Ciona301, Bee1, and Mosquito1 sequences were found within the vertebrate B clade, and like the vertebrate collagen genes of this clade, these invertebrate collagen genes have N-terminal TSPN domains (Aouacheria et al. 2004). Furthermore, the presence of insect and tunicate collagen genes among B/C vertebrate clade sequences points to the possibility that there were at least two, if not three, ancestral collagen types in the bilaterian ancestor. Both methods of tree reconstruction agreed well in overall topology and level of support with the exception of H. vulgaris. Parsimony places it with a bootstrap value of 87 in clade B/C, while in the Bayesian tree it is part of the A clade with a posterior probability of 99 (fig. 5). A comparison using the Templeton's Wilcoxon signed-rank test (Templeton 1983) of the placement of the Hydra collagen also shows incongruence in its position between the parsimony tree and the Bayesian tree. Comparing the parsimony consensus tree to the same topology, with only the position of Hydra changed, results in a statistically significant difference between them (P < 0.0001). Hydra's tendency to group with Ciona606 and Ciona916 in the parsimony tree is potentially due to long-branch attraction, a problem known to mislead parsimony analyses (Felsenstein 1978).
Collagen types I and II, which cluster in the A clade, are the most abundant collagen types in vertebrates (fig. 5). The hemichordate and lancelet collagen sequences in the A clade were found due to their transcript abundance in EST studies (Lowe et al. 2003; Panopoulou et al. 2003), so it is likely that these sequences represent the major fibrillar collagens found in these animals. It is also likely that these are the collagens identified in gill bars stained with chicken type II collagen monoclonal antibodies. It still remains to be seen whether or not more fibrillar collagens are present in the hemichordates, echinoderms, and lancelets. This will be answered in the near future as more of these organisms' genomes are sequenced and more ESTs become available.
Cartilaginous ECM containing collagen is typically thought of as a vertebrate-specific tissue type, although similar tissues have been described for many invertebrates (Cole and Hall 2004a, 2004b). Hemichordates and lancelets have pharyngeal cartilages that are structurally and chemically similar to vertebrate pharyngeal cartilages, so far as they are composed of collagen and proteoglycans. Despite the fact that different cell types secrete the cartilage matrix in hemichordates and lancelets versus vertebrates, it will be interesting to discover if similar gene pathways control the secretion of these ECM proteins.
Cartilaginous ECM appears to be endodermally derived in both hemichordates and lancelets. An invertebrate collagen similar to vertebrate type II collagen is an important component of the cartilage of hemichordates and lancelets. In addition, they secrete the matrix in such a way that the matrix-secreting cells themselves remain adjacent to, but are never inside, the matrix, which is different from the mode of cartilage formation found in vertebrates where chondrocytes are trapped within the matrix they secrete. Neural crest cartilages are found in the vertebrate pharyngeal gills and head, while the rest of the vertebrate cartilages are mesodermally derived from the sclerotome of somites. The types of proteoglycans present in hemichordate and lancelet gill bars remains to be determined. Hemichordates and lancelets share a similar benthic lifestyle, and it is possible that pharyngeal endodermal cartilage secretion is the ancestral mode of making cartilage in deuterostomes. In vertebrates, neural crest cells take on this role of pharyngeal cartilage secretion, but the developmental timing, place, and composition of the matrix may have stayed the same.
In summary, we have reviewed the chordate characteristics and have emphasized research on characteristics that are shared by chordates and hemichordates. The homologous pharyngeal gills of hemichordates, cephalochordates, and vertebrates are supported by collagenous cartilage skeletons. The similarity in formation and composition between hemichordate and cephalochordate gill bar matrix is striking, and it is likely that endodermally secreted acellular cartilage is the basal chordate pharyngeal cartilage. Further developmental work is critical to understanding the origin of the hemichordate stomochord and the possible patterning in the collar nerve chord.
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Supplementary Material |
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The sequence alignments in fasta and interleaved formats are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).
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Acknowledgements |
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Much of this work was funded by the University of Washington National Science Foundation ADVANCE program and the Department of Biology, and we gratefully acknowledge their support. S.E.S. was funded on a Howard Hughes Undergraduate Research Fellowship in the Swalla lab. A.L.R. was supported by a National Institutes of Health Developmental Biology Training Grant 5T32 HDO7183 and by the American Museum of Natural History Lerner-Grey Marine Research Fund. John Gerhart, Marc Kirchner, and Chris Lowe are thanked for the S. kowalevskii collagen clone. Sequencing was performed in the Biology Comparative Genomics Center, funded by a generous award from the Murdock Corporation.
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Footnotes |
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Laura Katz, Associate Editor
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References |
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