The lamprey: A jawless vertebrate model system for examining origin of the neural crest and other vertebrate traits

Abstract

Summary Lampreys are a group of jawless fishes that serve as an important point of comparison for studies of vertebrate evolution. Lampreys and hagfishes are agnathan fishes, the cyclostomes, which sit at a crucial phylogenetic position as the only living sister group of the jawed vertebrates. Comparisons between cyclostomes and jawed vertebrates can help identify shared derived (i.e. synapomorphic) traits that might have been inherited from ancestral early vertebrates, if unlikely to have arisen convergently by chance. One example of a uniquely vertebrate trait is the neural crest, an embryonic tissue that produces many cell types crucial to vertebrate features, such as the craniofacial skeleton, pigmentation of the skin, and much of the peripheral nervous system (Gans and Northcutt, 1983). Invertebrate chordates arguably lack unambiguous neural crest homologs, yet have cells with some similarities, making comparisons with lampreys and jawed vertebrates essential for inferring characteristics of development in early vertebrates, and how they may have evolved from nonvertebrate chordates. Here we review recent research on cyclostome neural crest development, including research on lamprey gene regulatory networks and differentiated neural crest fates.

Evolution of vertebrates as viewed from the crest

“…The order of character changes within a stem group is arbitrary. Adapted from Green and Bronner 98 .…”

Neural crest and the patterning of vertebrate craniofacial muscles

“…The neural crest (NCr)–myogenic mesoderm interaction story is, as espoused elegantly in Gans and Northcutt's () seminal review of 1983 (updated: Northcutt, ), central to the emergence of gnathostomes, and recent studies raise the possibility it may date back to the common ancestor of these fishes plus the cyclostomes (Gillis & Tidswell, ; Green & Bronner, ). Moveable gills and jaws created respiratory and food‐capture opportunities that enabled the explosive radiation of vertebrates, and neural crest cells are the major population contributing to their craniofacial connective tissues (reviewed by: Green, Simoes‐Costa, & Bronner, ).…”

A genome-wide assessment of the ancestral neural crest gene regulatory network

“…Importantly, we identify enhancer elements that drive expression in the premigratory and migratory neural crest of the lamprey, and provide evidence that regulation of a SoxE family gene is conserved between jawless and jawed vertebrates. By adapting high throughput tools to the lamprey, our data provide unique insight into the ancestral state of the neural crest GRN 20 .…”