Abstract
The sea lamprey is a basal, jawless vertebrate that possesses many neural crest derivatives, but lacks jaws and sympathetic ganglia. This raises the possibility that the factors involved in sympathetic neuron differentiation were either a gnathostome innovation or already present in lamprey, but serving different purposes. To distinguish between these possibilities, we isolated lamprey homologues of transcription factors associated with peripheral ganglion formation and examined their deployment in lamprey embryos. We further performed DiI labeling of the neural tube combined with neuronal markers to test if neural crest-derived cells migrate to and differentiate in sites colonized by sympathetic ganglia in jawed vertebrates. Consistent with previous anatomical data in adults, our results in lamprey embryos reveal that neural crest cells fail to migrate ventrally to form sympathetic ganglia, though they do form dorsal root ganglia adjacent to the neural tube. Interestingly, however, paralogs of the battery of transcription factors that mediate sympathetic neuron differentiation (dHand, Ascl1 and Phox2b) are present in the lamprey genome and expressed in various sites in the embryo, but fail to overlap in any ganglionic structures. This raises the intriguing possibility that they may have been recruited during gnathostome evolution to a new function in a neural crest derivative.
Highlights
IntroductionLampreys are agnathans (jawless vertebrates) that have many essential vertebrate characteristics but lack the sympathetic nervous system and jaws
Lampreys are agnathans that have many essential vertebrate characteristics but lack the sympathetic nervous system and jaws
While it has been established that lamprey lacks an organized sympathetic nervous system [14,19], some studies suggest that scattered sympathetic neurons and chromaffin cells might be associated with blood vessels, hindgut, cloaca and kidneys [15]
Summary
Lampreys are agnathans (jawless vertebrates) that have many essential vertebrate characteristics but lack the sympathetic nervous system and jaws. The only modern agnathans, are likely to be monophyletic, though there remains controversy on this point [3,4] As basal vertebrates, both occupy a critical phylogenetic position for understanding emergence of vertebrate traits. The peripheral nervous system of jawed vertebrates is comprised of sensory, parasympathetic, sympathetic and enteric ganglia that form clusters of neurons that innervate peripheral structures and relay information back to the central nervous system. All of these sensory and autonomic ganglia are derived from the neural crest, together with a contribution of cranial placodes to the sensory ganglia of the head [6]
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