Development of the viscerocranial skeleton during embryogenesis of the sea lamprey,<i>Petromyzon Marinus</i>

Martin, Wendy M.; Bumm, Lloyd A.; McCauley, David W.

doi:10.1002/dvdy.22164

Cited by 35 publications

(43 citation statements)

References 43 publications

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“…Embryos of P. marinus were reared as per the work by Martin et al (53). Plastic sections for P. marinus and L. japonicum were generated using JB-4 Plus (EM Sciences) according to the manufacturer's instructions and stained with toluidine blue or H&E.…”

Section: Methodsmentioning

confidence: 99%

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Tulenko

McCauley

MacKenzie

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Classical hypotheses regarding the evolutionary origin of paired appendages propose transformation of precursor structures (gill arches and lateral fin folds) into paired fins. During development, gnathostome paired appendages form as outgrowths of body wall somatopleure, a tissue composed of somatic lateral plate mesoderm (LPM) and overlying ectoderm. In amniotes, LPM contributes connective tissue to abaxial musculature and forms ventrolateral dermis of the interlimb body wall. The phylogenetic distribution of this character is uncertain because lineage analyses of LPM have not been generated in anamniotes. We focus on the evolutionary history of the somatopleure to gain insight into the tissue context in which paired fins first appeared. Lampreys diverged from other vertebrates before the acquisition of paired fins and provide a model for investigating the preappendicular condition. We present vital dye fate maps that suggest the somatopleure is eliminated in lamprey as the LPM is separated from the ectoderm and sequestered to the coelomic linings during myotome extension. We also examine the distribution of postcranial mesoderm in catshark and axolotl. In contrast to lamprey, our findings support an LPM contribution to the trunk body wall of these taxa, which is similar to published data for amniotes. Collectively, these data lead us to hypothesize that a persistent somatopleure in the lateral body wall is a gnathostome synapomorphy, and the redistribution of LPM was a key step in generating the novel developmental module that ultimately produced paired fins. These embryological criteria can refocus arguments on paired fin origins and generate hypotheses testable by comparative studies on the source, sequence, and extent of genetic redeployment.

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Section: Methodsmentioning

confidence: 99%

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Tulenko

McCauley

MacKenzie

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…In lamprey, the first and second arches, as well as the ventral pharynx, are supported by a cellular cartilage-like mesenchymal skeletal tissue called mucocartilage (Cattell et al, 2011;Johnels, 1948;Martin et al, 2009;Yao et al, 2011). Since lamprey mucocartilage also expresses FGFRs we asked what function FGF signaling might have in mucocartilage specification, differentiation or patterning.…”

Section: Research Articlementioning

confidence: 99%

“…Although lamprey possesses a head skeleton incorporating cellular cartilage it is thought to retain the basic structure and function of the head skeleton of early vertebrates. In contrast to the rigid, jointed cartilage elements of gnathostomes, the pharyngeal component of the lamprey head skeleton consists of thin rods of cellular cartilage that secrete an Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head extracellular matrix (ECM) made mainly of elastins and elastin-like proteins, with little fibrillar collagen, the main protein component of gnathostome cellular cartilage ECM (Martin et al, 2009;McBurney and Wright, 1996;McCauley, 2008;Robson et al, 1993;Yao et al, 2011). At the genetic level, although the lamprey head skeleton requires SoxE function to develop (Lakiza et al, 2011;McCauley and Bronner-Fraser, 2006), lamprey cellular cartilage does not express Runx or Barx, which are essential for gnathostome chondrogenesis (Cattell et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head

et al. 2014

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A defining feature of vertebrates (craniates) is a pronounced head supported and protected by a cellularized endoskeleton. In jawed vertebrates (gnathostomes), the head skeleton is made of rigid threedimensional elements connected by joints. By contrast, the head skeleton of modern jawless vertebrates (agnathans) consists of thin rods of flexible cellular cartilage, a condition thought to reflect the ancestral vertebrate state. To better understand the origin and evolution of the gnathostome head skeleton, we have been analyzing head skeleton development in the agnathan, lamprey. The fibroblast growth factors FGF3 and FGF8 have various roles during head development in jawed vertebrates, including pharyngeal pouch morphogenesis, patterning of the oral skeleton and chondrogenesis. We isolated lamprey homologs of FGF3, FGF8 and FGF receptors and asked whether these functions are ancestral features of vertebrate development or gnathostome novelties. Using gene expression and pharmacological agents, we found that proper formation of the lamprey head skeleton requires two phases of FGF signaling: an early phase during which FGFs drive pharyngeal pouch formation, and a later phase when they directly regulate skeletal differentiation and patterning. In the context of gene expression and functional studies in gnathostomes, our results suggest that these roles for FGFs arose in the first vertebrates and that the evolution of the jaw and gnathostome cellular cartilage was driven by changes developmentally downstream from pharyngeal FGF signaling.

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“…Modern dyelabeling (11) and gene expression (12) suggests that mucocartilage mesenchyme is derived from CNCC. Recent work has also revealed differences in the morphology of branchial basket chondrocytes (33), with those in the gill bars displaying a highly ordered "stack of coins" morphology, those in the dorsal-most horizontal (subchordal) cartilage bars appearing polygonal in shape, and those in the ventral-most horizontal (hypobranchial) cartilage bars forming irregular stacks. Furthermore, these populations likely form from separate dorsal, ventral, and intermediate chondrogenic condensations (34).…”

Section: Patterning In the Lamprey Pharynx Correlates With Differentmentioning

confidence: 99%

Evidence for the prepattern/cooption model of vertebrate jaw evolution

Cerny

Cattell²,

Sauka‐Spengler³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

107

179

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The appearance of jaws was a turning point in vertebrate evolution because it allowed primitive vertebrates to capture and process large, motile prey. The vertebrate jaw consists of separate dorsal and ventral skeletal elements connected by a joint. How this structure evolved from the unjointed gill bar of a jawless ancestor is an unresolved question in vertebrate evolution. To understand the developmental bases of this evolutionary transition, we examined the expression of 12 genes involved in vertebrate pharyngeal patterning in the modern jawless fish lamprey. We find nested expression of Dlx genes, as well as combinatorial expression of Msx, Hand and Gsc genes along the dorso-ventral (DV) axis of the lamprey pharynx, indicating gnathostome-type pharyngeal patterning evolved before the appearance of the jaw. In addition, we find that Bapx and Gdf5/6/7 , key regulators of joint formation in gnathostomes, are not expressed in the lamprey first arch, whereas Barx , which is absent from the intermediate first arch in gnathostomes, marks this domain in lamprey. Taken together, these data support a new scenario for jaw evolution in which incorporation of Bapx and Gdf5/6/7 into a preexisting DV patterning program drove the evolution of the jaw by altering the identity of intermediate first-arch chondrocytes. We present this “Pre-pattern/Cooption” model as an alternative to current models linking the evolution of the jaw to the de novo appearance of sophisticated pharyngeal DV patterning.

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Development of the viscerocranial skeleton during embryogenesis of the sea lamprey,Petromyzon Marinus

Cited by 35 publications

References 43 publications

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head

Evidence for the prepattern/cooption model of vertebrate jaw evolution

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