Evolution of neural crest and placodes: amphioxus as a model for the ancestral vertebrate?

Abstract

Recent studies of protochordates (ascidian tunicates and amphioxus) have given insights into possible ancestors of 2 of the characteristic features of the vertebrate head: neural crest and placodes. The neural crest probably evolved from cells on either side of the neural plate-epidermis boundary in a protochordate ancestral to the vertebrates. In amphioxus, homologues of several vertebrate neural crest marker genes (BMP2/4, Pax3/7, Msx, Dll and Snail) are expressed at the edges of the neural plate and/or adjacent nonneural ectoderm. Some of these markers are also similarly expressed in tunicates. In protochordates, however, these cells, unlike vertebrate neural crest, neither migrate as individuals through embryonic tissues nor differentiate into a wide spectrum of cell types. Therefore, while the protochordate ancestor of the vertebrates probably had the beginnings of a genetic programme for neural crest formation, this programme was augmented in the earliest vertebrates to attain definitive neural crest. Clear homologues of vertebrate placodes are lacking in protochordates. However, both amphioxus and tunicates have ectodermal sensory cells. In tunicates these are all primary neurons, sending axons to the central nervous system, while in amphioxus, the ectodermal sensory cells include both primary neurons and secondary neurons lacking axons. Comparisons of developmental gene expression suggest that the anterior ectoderm in amphioxus may be homologous to the vertebrate olfactory placode, the only vertebrate placode with primary, not secondary, neurons. Similarly, biochemical, morphological and gene expression data suggest that amphioxus and tunicates also have homologues of the adenohypophysis, one of the few vertebrate structures derived from nonneurogenic placodes. In contrast, the origin of the other vertebrate placodes is very uncertain.

Vertebrate Cranial Placodes as Evolutionary Innovations—The Ancestor's Tale

“…These cells or subsets of them also express the Achaete-scute homologue Ash, Tlx, Hu/Elav, Islet, COE, POU4, SoxB1, Six1/2, Six4/5, Eya, and Delta (Benito-Gutierrez, Illas, Candiani et al, 2006;Holland & Holland, 2001;Kaltenbach, Yu, et al, 2009;Kozmik et al, 2007;Lu, Luo, & Yu, 2012;Mazet, Masood, Luke, Holland, & Shimeld, 2004;Meulemans & Bronner-Fraser, 2007;Rasmussen, Holland, Schubert, Beaster-Jones, & Holland, 2007;Satoh, Wang, Zhang, & Satoh, 2001;Schubert et al, 2004), while expression of Atonal has not been described. With this expression profile, these sensory cells resemble various placodally derived sensory cells or sensory neurons, but no one to one correspondence can be established .…”

“…These are usually ciliated and surrounded by a collar of microvilli, but the number of cilia and microvilli and their arrangement is variable between cells and taxa (Burighel, Caicci, & Manni, 2011;Holland & Holland, 2001). In the absence of direct experimental evidence for the sensory modality mediated by these receptors, it can only be tentatively assigned as chemosensory or mechanosensory based on ultrastructure.…”

“…The rostral ectoderm also harbors primary sensory cells expressing vertebrate type odorant GPCRs (Satoh, 2005), while Hatschek's pit expresses Pit1, Lhx, Islet as well as Six1/2 and Eya and gives rise to neurosecretory cells (Candiani, Holland, Oliveri, Parodi, & Pestarino, 2008;Jackman, Langeland, & Kimmel, 2000;Kozmik et al, 2007;Wang, Zhang, Yasui, & Saiga, 2002). Due to their position and gene expression patterns, the rostral ectoderm has been suggested to be a homologue of the olfactory placode (Glardon et al, 1998;Holland & Holland, 2001) and Hatschek's pit a homologue of the adenohypophyseal placode (Boorman & Shimeld, 2002;Nozaki & Gorbman, 1992;Yasui et al, 2000).…”

“…These usually occur as scattered single cells although a few sense organs composed of small clusters of sensory cells (e.g., the rostral corpuscles of de Quatrefages) are also present. Both primary and secondary sensory cells with cilium and microvillar collar have been described and classified as putative chemo-or mechanoreceptors (e.g., Holland & Holland, 2001;Lacalli, 2004;Lacalli & Hou, 1999;Ruppert, 1997).…”

Retention of genes involved in the adenohypophysis-mediated endocrine system in early vertebrates

“…Amphioxus has Hatschek's pit (Gorbman et al, 1999), which likely is homologous to Rathke's pouch (the adenohypophysis primordium) of vertebrates because of the similar developmental processes of these organs (Holland and Holland, 2001). This indicates that a Rathke's pouch-like (or Hatschek's pit-like) ancestral organ has already existed in the common ancestor of vertebrates and cephalochordates.…”