A lamprey from the Devonian period of South Africa

107

179

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.

“…S1). This unjointed arrangement is similar to that seen in the fossil agnathans (14,15), and is thought to reflect the ancestral vertebrate condition.…”

mentioning

confidence: 57%

Evidence for the prepattern/cooption model of vertebrate jaw evolution

Cerny

Cattell²,

Sauka‐Spengler³

et al. 2010

107

179

“…The presence of such "lingual" cartilage has been asserted only in extant lampreys and hagfishes (26), but also suggested in euphaneropids (34) and fossil lampreys (35,36). Hence, even if it is supported by indirect evidence and not by actual cartilage remains or imprints that future investigations may reveal, our reconstruction lends strong support to a vertebrate affinity of conodonts as stem cyclostomes or possibly as the most "primitive" stem gnathostomes (i.e., between lampreys and "ostracoderms") (Fig.…”

Section: Discussionmentioning

confidence: 99%

Synchrotron-aided reconstruction of the conodont feeding apparatus and implications for the mouth of the first vertebrates

Goudemand

Orchard

Urdy

et al. 2011

The origin of jaws remains largely an enigma that is best addressed by studying fossil and living jawless vertebrates. Conodonts were eel-shaped jawless animals, whose vertebrate affinity is still disputed. The geometrical analysis of exceptional three-dimensionally preserved clusters of oro-pharyngeal elements of the Early Triassic Novispathodus, imaged using propagation phase-contrast X-ray synchrotron microtomography, suggests the presence of a pulley-shaped lingual cartilage similar to that of extant cyclostomes within the feeding apparatus of euconodonts ("true" conodonts). This would lend strong support to their interpretation as vertebrates and demonstrates that the presence of such cartilage is a plesiomorphic condition of crown vertebrates.apical cartilage | conodont oral skeleton | early vertebrates | homology H ow the transition from "agnathans" to gnathostomes ("jawed" vertebrates) occurred is one of the most intriguing problems of evolutionary biology (1). Little is known about the endoskeleton of fossil jawless vertebrates [e.g., fossil cyclostomes (hagfishes and lampreys) and "ostracoderms"]. Although the view is still debated (2), euconodonts would have possessed the very first vertebrate mineralized skeleton in the form of their oral denticles (3, 4).The general architecture of the conodont oral skeleton is a bilaterally symmetrical array of usually 15 phosphatic elements, which generally becomes disarticulated after the decay of the supporting tissues. Hence most conodonts are known only as isolated elements. From the detailed study of hundreds of articulated "natural assemblages" and photographic simulation of their collapse, Purnell and Donoghue (5) constructed a 3D model of the Idiognathodus apparatus [presumably a template for all ozarkodinid apparatuses (6)] in which one pair of obliquely pointed M elements are located rostrally and, behind them, one unpaired S 0 (subscript number indicates distance ordering from the symmetry axis) element lying on the axis of bilateral symmetry and four pairs of elements (S 1-4 ) located on both sides of the S 0 would have grasped food and, more caudally, two pairs of pectiniform elements (P 1 , P 2 ) would have processed this food by crushing and/or slicing (5, 7, 8) ( Fig. 1 A-B) (for "standard" orientation of single elements, see Fig. S1). Purnell and Donoghue's reconstruction of a generalized resting (dead) position is very well supported and in most aspects very convincing. It is therefore adopted here as a basis upon which we build our dynamic reconstruction of the feeding apparatus at work.How could these elements actually grasp or cut prey tissues? Purnell and Donoghue's functional model (section 6 of ref. 5) was based chiefly on analogies with extant agnathans. Indeed, the "quite simple" geometry of the Idiognathodus elements does not provide much indication of what motions are possible or not [except for uncommon natural assemblages (see below)]. Thus, hypotheses were inferred from extant putative closest relatives. In our view, the more "compli...

“…Because of its parasitic lifestyle, the lamprey body plan may not reflect that of the early chordate ancestor. However, it is interesting to note that modern lampreys closely resemble lamprey fossils Ͼ360 million years old (21), suggesting that their body plan has remained fixed. This raises the intriguing possibility that the core modules of the NC-GRN of a modern lamprey may reflect the ancestral vertebrate state.…”

mentioning

confidence: 99%

Dissecting early regulatory relationships in the lamprey neural crest gene network

Nikitina

Sauka‐Spengler²,

Bronner‐Fraser³

2008

The neural crest, a multipotent embryonic cell type, originates at the border between neural and nonneural ectoderm. After neural tube closure, these cells undergo an epithelial-mesenchymal transition, migrate to precise, often distant locations, and differentiate into diverse derivatives. Analyses of expression and function of signaling and transcription factors in higher vertebrates has led to the proposal that a neural crest gene regulatory network (NC-GRN) orchestrates neural crest formation. Here, we interrogate the NC-GRN in the lamprey, taking advantage of its slow development and basal phylogenetic position to resolve early inductive events, 1 regulatory step at the time. To establish regulatory relationships at the neural plate border, we assess relative expression of 6 neural crest network genes and effects of individually perturbing each on the remaining 5. The results refine an upstream portion of the NC-GRN and reveal unexpected order and linkages therein; e.g., lamprey AP-2 appears to function early as a neural plate border rather than a neural crest specifier and in a pathway linked to MsxA but independent of ZicA. These findings provide an ancestral framework for performing comparative tests in higher vertebrates in which network linkages may be more difficult to resolve because of their rapid development.neural plate border ͉ transcription factor ͉ agnathan