Abstract
Neural crest and placodes are key innovations of the vertebrate clade. These cells arise within the dorsal ectoderm of all vertebrate embryos and have the developmental potential to form many of the morphological novelties within the vertebrate head. Each cell population has its own distinct developmental features and generates unique cell types. However, it is essential that neural crest and placodes associate together throughout embryonic development to coordinate the emergence of several features in the head, including almost all of the cranial peripheral sensory nervous system and organs of special sense. Despite the significance of this developmental feat, its evolutionary origins have remained unclear, owing largely to the fact that there has been little comparative (evolutionary) work done on this topic between the jawed vertebrates and cyclostomes—the jawless lampreys and hagfishes. In this review, we briefly summarize the developmental mechanisms and genetics of neural crest and placodes in both jawed and jawless vertebrates. We then discuss recent studies on the role of neural crest and placodes—and their developmental association—in the head of lamprey embryos, and how comparisons with jawed vertebrates can provide insights into the causes and consequences of this event in early vertebrate evolution.
Highlights
The vertebrate head is a complex tapestry of morphological features woven together during embryonic development from a varied array of specialized cell types
We focus on recent work describing the developmental association of neural crest and placodes in the head of jawless vertebrate embryos and how these studies, when placed within a comparative embryology framework, can provide important clues as to how the intimate relationship between these unique cell populations first evolved in early vertebrates
Similar to that described in multiple jawed vertebrate model systems, lampreys express orthologs of Six1/2 in the otic vesicle, posterior lateral line, and epibranchial placodes and Phox2 in epibranchial ganglia, which are presumably derived in part from placodes (Häming et al, 2011; Green et al, 2017; Hockman et al, 2017; York et al, 2019b)
Summary
The vertebrate head is a complex tapestry of morphological features woven together during embryonic development from a varied array of specialized cell types. Some of the features in the vertebrate head are derived from populations of cells that are evolutionarily ancient, and not unique to vertebrates (e.g., mesoderm and endoderm), there are two notable exceptions to this observation—the neural crest and placodes (Gans and Northcutt, 1983; Couly et al, 1993; Santagati and Rijli, 2003; Kuratani, 2008; Square et al, 2016b; Hall, 2018; Kuratani and Ahlberg, 2018; Cheung et al, 2019). Both neural crest cells and placodes are found only in vertebrate animals and they are responsible for constructing many of the traits that uniquely define the vertebrate clade (Figure 1), including the cartilage and bone of the head and jaw skeleton, neurons and glia of the peripheral sensory nervous system, colorful patterns of pigmentation, and much more (Green et al, 2015; Ziermann et al, 2018; Fish, 2019; Martik et al, 2019; Vandamme and Berx, 2019; York and McCauley, 2020b)
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