Developmental origins and evolution of jaws: new - PubMed Open Access https://doi.org/10.1038/sj.hdy.6800205, DOI: https://doi.org/10.1038/sj.hdy.6800205. How did vertebrates first evolve jaws? - USC Stem Cell J Craniofac Genet Dev Biol. Recently, Soukup et al. Soc. Ninety-seven percent of the support for the eLife study came from federal funding from the National Institute of Dental and Craniofacial Research (grants R35DE027550, F31DE030706, and K99DE029858). J. Vertebr. CAS Now, two new studies published in the journals eLife and Development look at the origins of these jaws. Evolution of the vertebrate jaw from developmental perspectives Evol. P. nigra is a species with extremely large numbers of teeth on both the oral and pharyngeal jaws; thus the inclusion of P. nigra may have disproportionate affects on the regression trend. 257, 289307 (2003), Johanson, Z. The Evolutionary Emergence of Vertebrates From Among Their Spineless and P.C.J.D. The two exceptions are provided by pax9 and barx1. Oral and pharyngeal tooth development is generally governed by the same genetic regulators (see Figures 4 and 5); this corresponds to a positive correlation in the number of tooth units across the two disparate sites (tooth number regulation; see Figure 2). This was accompanied by the loss of some genes occupying the ancient gene network, including the hox genes and barx1 (Barx1 was then regained in mammalian molar formation); Placoderms (the earliest jawed vertebrates) evolved an oral dentition independently in derived groups [74]; however, we suggest that the networks are common for teeth and were in place prior to the advent of oral jaws. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. and the Paul Scherrer Institut (P.C.J.D.). (B, E, H, K, N, and O) are all to the same scale: scale bars represent 100 m. How did vertebrates first evolve jaws? -- ScienceDaily Accessibility Comment on Separate evolutionary origins of teeth from evidence in fossil jawed vertebrates. ISSN 1365-2540 (online) Biol Open. Point B indicates the origin of oral jaws in concert with the co-option of the core dental gene network allowing the development of teeth on the recently acquired oral jaws. pax9 is not essential for vertebrate tooth development (it is not expressed in all teeth), although it is necessary for mammalian odontogenesis [65,66]. Regionalized signaling in an enamel organ such as that originating from the enamel knot has been purposely omitted from this generalized diagram. Yes constructed the neoclassical hypothesis (Mallatt, 1996) mainly from the comparative and functional morphology of post-embryonic and adult fishes. The authors declare no competing financial interests. Genes Dev 13: 31363148. Reports of both histological and cell labeling evidence have suggested that some vertebrates develop oral teeth in close proximity to endodermal cells, even mammalian incisors [37] and molars (P. Sharpe, personal correspondence). Biological processes are seldom simple, but this work shows that even something as complex as the development of a jaw can be understood as a series of much more simple developmental steps. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. The images reveal that Placoderms did have true teeth, with dentine and pulp cavities, and a distinct mode of tooth replacement. Development and evolution of the tetrapod skull-neck boundary. How did the development of jaws affect vertebrates? R1, row 1; R2, row 2. The available data are thus equivocal on the molecular regulation of oral versus pharyngeal dentitions. A zebrafish showing, from left to right, the eye, the pseudobranch, and the gills (Image by Peter Fabian/Crump Lab). How this axis is established is still debated, but like limbs it clearly involves Dlx homeobox transcription factors related to distalless, a key regulator of appendage development in Drosophila. Nearly all fishes possess a tiny anatomical structure called a pseudobranch, which resembles a vestigial gill. Thus, a combination of cell intrinsic (Dlx) and extrinsic (Fgf8) factors is probably required to establish the skeletal pattern. (PDF 11463 kb), Rcklin, M., Donoghue, P., Johanson, Z. et al. Trumpp A, Depew MJ, Rubenstein JL, Bishop JM, Martin GR (1999). How did vertebrates first evolve jaws? - Keck School of Medicine of USC Biol. No, Is the Subject Area "Gene expression" applicable to this article? In the absence of clear fossil evidence, the eLife publication presents living evidence in support of the theory that jaws originated from gills. Clipboard, Search History, and several other advanced features are temporarily unavailable. The scientists confirmed that in the study organism, zebrafish, gills and jaws arise from the same embryonic structures, called the pharyngeal arches. The first arch gives rise to the jaw and is called the mandibular while the other arches become gills. This is in contrast to its expression in mammalian teeth where it is exclusively expressed in the epithelial cells of the intergerm space (ZOI) before its expression is recruited into the tooth during morphogenesis of the outer dental epithelium [52,53]. Introduction. the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Yes Therefore, it is intriguing to speculate that Hox and barx1 expression were components of an ancient dental program deep in the pharynx of jawless fishes, retained in the pharyngeal teeth of extant fishes. CAS BMC Ecol Evol. Some vertebrates have lost the entire oral dentition (birds, turtles, etc. Although tooth-like elements (denticles) were also present on the dermal surface of some agnathans (including thelodonts) and chondrichthyans, it was the occurrence of uniquely patterned pharyngeal teeth in agnathans that likely foreshadowed all other vertebrate oropharyngeal teeth [1,35]. It is notable that members of the core dental network are coexpressed in the development of other vertebrate organs such as scales, feathers, and hairs [54,56,8086] and that the origin of these gene families predate vertebrates altogether. We thank S. Bengtson, J. Cunningham, D. Murdock, S. Giles and A. Hetherington for help at the TOMCAT beamline; K. Robson-Brown for help at the Micro-CT, and H. Llivre and G. Clment for loan of specimens. Scale bar in (C) represents 20 m. E-mail: gareth.fraser@biology.gatech.edu (GJF); todd.streelman@biology.gatech.edu (JTS), Affiliation Introduction Jawed vertebrates, or gnathostomes, represent the majority of extant vertebrate species. We interpret these data to hold important implications for the first vertebrate dentition, and the origin of an ancient dental gene network, retained in pharyngeal endoderm of modern fishes and modified for teeth on oral jaws (Figures 6 and 7). Scale bar in (B) represents 100 m; (B, E, C, and F) are all to the same scale. There are also anatomical similarities: the gills are supported by upper and lower bones, which could be thought of as analogous to the upper and lower jaws. In addition to genes described here, a number of others expressed in the pharyngeal dentition of teleosts are part of the ancient dental network, including eve1 [41,69], lhx6, and lhx7 [43] (Figure 7; Table 1). Point A indicates the origin of the ancient dental gene network and pharyngeal teeth in extinct () jawless fish. (K and L) show bmp2 expression in MZ. Anterior gill bars evolved into the jaw, which supports structures in vertebrates. Cartilage of the vertebrate jaw is derived from cranial neural crest cells that migrate to the first pharyngeal arch and form a dorsal "maxillary" and a ventral "mandibular" condensation. , (DF) hoxA5a (A5a) expression in C. conophorus (CC). The evolutionary origin of toothed oral jaws galvanized the dominance of gnathostomes and may have been prompted by the loss of Hox gene regulation in PA1 [21,22]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Synchrotron X-ray tomographic microscopy of fossil embryos. We find that tooth number is coordinately regulated on pharyngeal versus oral jaws across a broad diversity of Lake Malawi cichlids (Figure 2). Our studies show that the mandibular arch contains the basic machinery to make a gill-like structure, said Crump, the eLife studys corresponding author, and a professor of stem cell biology and regenerative medicine at the Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research at USC. Dorsal views of (B, E, and H) show adult lower oral jaws, cleared and alizarin-stained bone/dentine preparation, and (C, F, and I) show adult lower (ceratobrachial [CB]5/PA7) pharyngeal jaws with the soft tissue removed. -catenin, fgf3, fgf10, and notch2, a set of stem cell markers recruited during cichlid oral jaw tooth replacement (G. J. Fraser and J. T. Streelman, unpublished data) are also assigned to the ancient dental network, based on expression in pharyngeal teeth (Figure 7; Table 1). Analyses were run with untransformed tooth number because the correlation of species values suggested the variance was equal for species possessing both large and small numbers of teeth. Together, these two studies point to a pseudobranch being present in the last common ancestor of all jawed vertebrates, said study co-author J. Andrew Gillis. In the absence of clear fossil evidence, the eLife publication presents living evidence in support of the theory that jaws originated from gills. During the early evolution of vertebrates, the appearance of a pharyngeal dentition greatly enhanced the capacity for processing food. This formidable pharyngeal machinery for food processing can produce enough force in some species to crush hard prey such as shelled molluscs [6,7]. Genes Dev 16: 10891101. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Teeth and jaws constitute a model of the evolutionary developmental biology concept of modularity 1 and they have been considered the key innovations underpinning a classic example of adaptive. Amphibians were the first tetrapod vertebrates as well as the first vertebrates to live on land. The new study also revealed exciting new evidence for at least two important signaling centers in an arch field. GJF and JTS wrote the paper. In the meantime, to ensure continued support, we are displaying the site without styles (C and D) show barx1 expression in LF. dlx2 labels the first tooth (in the series) for each tooth row in both the oral jaw (PA1, black arrowhead in [O]) and the pharyngeal jaw (PA7, black arrowheads in [P]). Embryo ages (in days postfertilization [dpf]) were set after the identification of mouth brooding females (day 0). Colors in (A) correspond to those in (B). ISSN 0018-067X (print). The evolution of the jaw is recorded in fossil remains and in living cartilaginous fishes and bony fish, with a focus on the major changes in patterning of jaw elements between taxa, leading to the evolution of land-dwelling vertebrates. 10 August 2017, Receive 51 print issues and online access, Prices may be subject to local taxes which are calculated during checkout, Atchley, W. R. & Hall, B. K. A model for development and evolution of complex morphological structures and its application to the mammalian mandible. In epithelial thickenings, bmp2 is present in the thickened epithelial cells and is also expressed in the condensing cells of the underlying mesenchyme (black arrowheads). Before (I) pitx2 marks the dental-competent oral epithelium around the tooth sites and is up-regulated in tooth germs, from the thickened epithelium to the maturing tooth germ (black arrowheads). To obtain We integrate these molecular data with comparative morphology and paleontology to (1) infer the ancient dental network used to pattern the first teeth and (2) suggest a core regulatory circuit common to all dentitions. sharing sensitive information, make sure youre on a federal Jawed vertebrates arose from non-jawed vertebrates that had a pharyngeal gill apparatus composed of gill bars and slits. Even the developmental teleost model, the zebrafish (Danio rerio), has a reduced dentition with few teeth present on the lower PA7 and a complete loss of oral teeth [30,31]. In a new pair of studies in eLife and Development, scientists reveal clues about the origin of this thrilling evolutionary innovation in vertebrates. A second, unexpected signaling center must lie near the center of the arch field, since the transformations produced by loss of Dlx5 and Dlx6 functions are mirror-image duplications along the PD axis (intrasegmental duplicates of the upper jaw). (K) bmp2 is localized to the epithelial tooth thickenings (black arrowheads) and the competent epithelia along the mesiodistal axis of the oral jaw. All animals were handled in strict accordance with good animal practice as defined by the relevant national and/or local animal welfare bodies, and all animal work was approved by the appropriate committee at Georgia Institute of Technology. Zool. In many respects, these interactions resemble those that occur between the apical ectodermal ridge and mesenchyme of the limb bud, where Dlx genes are also required. Surprisingly, we find that both palatoquadrate and Meckel's cartilage derive solely from the ventral "mandibular" condensation. The History of Animal Evolution - University of Waikato official website and that any information you provide is encrypted These dentitions are evolutionarily decoupled; teeth arose first in the pharynx prior to the origin of jaws. 2004 Dec 1;276(1):207-24. doi: 10.1016/j.ydbio.2004.08.045. Developmental origins and evolution of jaws: new interpretation of Subsequently in some groups of advanced teleost fishes [69], including cichlids, the ancient dental network located on PA7, in coordination with a recent adaptation of the pharyngeal skeleton, led to the evolution of a new functional toothed jaw, the pharyngeal jaw. https://doi.org/10.1371/journal.pbio.1000031, Academic Editor: Jukka Jernvall, University of Helsinki, Finland, Received: June 30, 2008; Accepted: January 5, 2009; Published: February 10, 2009. During development, jaws and gills both arise from embryonic structures called pharyngeal arches. The first of these arches is called the mandibular arch because it gives rise to jaws, while additional arches develop into gills. B 279, 775779 (2012), Smith, M. M. The pattern of histogenesis and growth of tooth plates in larval stages of extant lungfish. eda is expressed during gill raker initiation similar to its expression in teeth (Figure 5E and 5F; [49]), labeling the interraker mesenchyme region for each gill raker primordium (Figure 5D and 5F). By submitting a comment you agree to abide by our Terms and Community Guidelines. Pharyngeal tooth counts were performed on high-magnification images of Malawi cichlid lower pharyngeal jaws, and each tooth was counted (see Figure 2). This suggests that PA7 has unique properties separating it from more anterior arches. How and when did jaws evolve? Earth.com The odontode explosion: the origin of tooth-like structures in vertebrates. The second arch (PA2) forms the hyoid and the jaw support; the remaining posterior arches either contribute to the formation of the gills and gill-related skeletal structures (branchial) in fish or become incorporated into the throat of tetrapods [15]. However, their evolutionary origins are much debated. Thus it is intriguing to note lack or the simplified peripheral oral dentition in the first gnathostomes (e.g., derived placoderms [7375]), an experimental dental transition. Significantly, mice that lose the function of some Hox genes undergo intersegmental mirror-image duplications along the AP axis, suggesting that this may be a common aspect of homeotic duplications of adjacent fields of cells in vertebrates. (K and L) show a coronal section: (K) hoxB6b expression surrounds each tooth in the dental mesenchymal cells (black arrowheads); stronger expression is observed at the base of each tooth unit (black arrow), possibly related to the attachment between the mineralized tooth and the underlying cartilage of CB5. Simeone et al (1994). Again, at this stage there are nested patterns of transcription factors expressed within an arch field, notably genes of the Dlx family. Open Access (D, E, and F) show eda in the lower pharyngeal elements of M. zebra (MZ) (7dpf); dorsal views. https://doi.org/10.1371/journal.pbio.1000031.g006. Scale bar in (J) represents 100 m. Epub 2020 Aug 21. Human mutations in these and other members of the ectodysplasin pathway cause various forms of hypohidrotic ectodermal dysplasia (HED), which manifests by specifically affecting ectodermal appendages [52]. This ancient dental regulatory circuit has been conserved in modern fishes as those markers expressed in pharyngeal dentitions. Abbreviations: (A and B) Oral jaw (PA1, lilac) houses a dentition (dark-blue circles) that develops in an ectoderm-influenced environment; dashed line in (A) represents the ectoderm/endoderm interface; a strict boundary may not exist due to cell mixing across this interface [36]. Open Access articles citing this article. A jaw-dropping conundrum: Why do mammals have | EurekAlert! To read more about these two papers and evo-devo research, visit https://www.mbl.edu/news/evolution-evo-devo. Furthermore, later in development, these elements house an additional set of teeth/denticles (unpublished data) [39,57,58]. Scale bars in (A and D) both represent 100 m. An official website of the United States government. This dashed line also reflects the border between Hox genepositive and Hox genenegative oropharyngeal regions among vertebrates; we do not suggest a functional relationship between the two. (D, F, H, J, N, and P) show dorsal views of the developing lower pharyngeal dentition; (B and L) are coronal sections through the pharyngeal teeth. These findings showed that teeth and jaws did not evolve together, contradicting earlier theories. The teeth are composed of dentine and bone, and show a distinct pulp cavity that is infilled centripetally as development proceeds. Lee SH, Bdard O, Buchtov M, Fu K, Richman JM. Depew MJ et al (1999). Here, we have combined paleontology, molecular developmental biology, and comparative morphology to infer the developmental basis of ancient dental structures close to the origin of vertebrates and their evolutionary progression through time to recent diversity. One of these features, the pharyngeal slits, is believed to be the origin of the hinged jaw that allows us to do so much with our mouths. We infer from these data that the transition from agnathans to the first gnathostomes coincided with further modifications of the dental network governing the development of the early oral dentition. However, different pairs of Dlx genes differ in where they are expressed, that is, their expression domains. Oral tooth number was estimated based on the exact numbers of teeth on one half of the lower jaw first row, multiplied by the exact number of rows, multiplied by 2 (for the two halves of the oral jaw process; Figure 2). (D) is composed of two images of the same specimen; the boxed area of the oral jaw (separate image) is shown in (E). (A, C, E, G, I, K, M, and O) are all to the same scale. Does not have vertebrae Major difference between a hagfish and more evolved vertebrates is that Weight is less than the upward force of the water Organisms that live in or on water are buoyant when their A fan shaped array of bones Data points labeled DC, MZ, and LF refer to the three species in (AI). There is avid interest in understanding the origin and developmental control of the dentition [1,35,39,59,60]. M. zebra (MZ) (A, B, and IN) and L. fuelleborni (LF) (CH, O, and P) are represented here at the three to four oral tooth stage (67 dpf); the pharyngeal dentition develops ahead of the oral teeth, and so at this time point there are approximately seven pharyngeal teeth per pharyngeal quadrant. Locally released retinoic acid repatterns the first branchial arch cartilages in vivo. The first pharyngeal arch (PA1) in the series forms the oral jaws (Figure 1). This relatively simple code of positional information determines the emergence of the segmental complexity of the head skeleton. We identify Hox genes as important components of an ancient dental gene-regulatory circuit and pinpoint subsequent modifications to this gene network that accompanied the evolution of toothed oral jaws. No, PLOS is a nonprofit 501(c)(3) corporation, #C2354500, based in San Francisco, California, US, Corrections, Expressions of Concern, and Retractions, https://doi.org/10.1371/journal.pbio.1000031. Our studies show that the mandibular arch contains the basic machinery to make a gill-like structure, said eLife study co-author Gage Crump, a professor at University of Southern California. pax9 (Pax9) is imperative for mammalian tooth development, expressed during cichlid (Figures 4 and 6 and Table 1; [49]) and Mexican tetra [31] oral tooth initiation, but not expressed in relation to the pharyngeal teeth of cichlids (Figure 4) and zebrafish [43]. Attainment of the biting jaw is regarded as one of the major novelties in the early history of vertebrates. eda is in brackets due to the differential expression between fish (mesenchyme) and mammals (epithelium). After color reaction (NBT/BCIP; Roche) embryos were washed in PBS and fixed again in 4% PFA, before whole-mount imaging using a Leica Microsystems stereo microscope (MZ16). [101]. Homologous pharyngeal arch segments are numbered 17; skeletal elements and the Dlx genes they express are color-coded (red=dorsal; blue=intermediate; yellow=ventral). Chew on this: we finally know how our jaws evolved - The Conversation DC, MZ, and LF represent a range in oral and pharyngeal tooth number (Table S1): there are fewest teeth in DC, more teeth in MZ, many teeth in LF. One question the new study suggests is: What are the molecular pathways through which Dlx genes confer positional identities to cells in the jaw? Ordered dentitions are an integral feature of gnathostome oral jaws; most extant gnathostome groups do not possess pharyngeal teeth. Gill rakers will feature a secondary tooth/denticle set later in development. Heredity In a new pair of studies in eLife and Development, scientists reveal clues about the origin of this thrilling evolutionary innovation in vertebrates. volume90,pages 35 (2003)Cite this article. Using elegant imaging and cell tracing techniques in zebrafish, Thiruppathy and her colleagues conclusively showed that the pseudobranch originates from the same mandibular arch that gives rise to the jaw. Specimens for in situ hybridization were anesthetized in tricaine methanesulfonate (MS222; Argent) and fixed overnight in 4% paraformaldehyde (PFA) in 0.1% phosphate-buffered saline (PBS) at 4 C. Depew et al (2002) and his colleagues in a new article published in Science take our understanding a step further. This implies that the structures arising from the mandibular archthe pseudobranch and the jawmight have started out as gills that were modified over the course of deep evolutionary time., Gillis, who is the corresponding author of the Development study and a co-author on the eLife study, added: Together, these two studies point to a pseudobranch being present in the last common ancestor of all jawed vertebrates. (J) Across Malawi cichlids, a positive correlation is observed between the number of teeth on the oral and pharyngeal jaws (r = 0.53 without P. nigra and r = 0.66 including P. nigra; p < 0.00001), see (AI). At first glance, jaw formation seems extremely complex. J Craniofac Genet Dev Biol. [36] lead to the interpretation that most anterior oral teeth are likely ectodermal, posterior oral teeth develop from a mixed population of ectodermal and endodermal epithelia, and the most posterior teeth, such as those on PA7 in teleost fishes, are likely formed from strictly endodermal cells [1,5,34]. This observation prompts a series of related questions: what role, if any, do Hox genes play in the pharyngeal dentition? A true head represents one of the most sophisticated anatomical structures in vertebrates and is arguably one of the most significant drivers of vertebrate success (Northcutt, 2005; Wilkie & Morriss-Kay, 2001).The evolution of a protective cranium may have also contributed to the emergence of a complex brain and senses. 66, 101157 (1991), Article 306, 183203 (2006), rvig, T. Acanthodian dentition and its bearing on the relationships of the group. Gnathostomes or "jaw-mouths" are vertebrates that possess jaws. It is these expression domains that divide up the arch field into zones, which appear to correspond to individual bones (Figure 1). J. Linn. Unable to load your collection due to an error, Unable to load your delegates due to an error, Collaborators, These developmental and anatomical observations led to the theory that the jaw evolved by modification of an ancestral gill, said Thiruppathy. Peter Fabian, a postdoctoral trainee in the Crump Lab at USC, is also a co-author on the eLife study. Philos. Correspondence to EB4, epibranchial 4; pc, pharyngeal cavity. Eusthenopteron. Parker H. Petit Institute for Bioengineering and Biosciences and School of Biology, Georgia Institute of Technology, Atlanta, Georgia, United States of America, Affiliations The break down of the stomodeum or the oropharyngeal/buccopharyngeal membrane leads to mixing of both anterior ectodermal and posterior endodermal cells within the oropharyngeal cavity, therefore a definite ectoderm/endoderm boundary may be unidentifiable. (M) hoxD4a is expressed in the hindbrain (black arrow) and in the posterior pharyngeal mesenchyme (white arrowhead). Initiation of the mouse dentition is unaffected when Hoxa2 is overexpressed in the first arch [22].