May 1, 2014;
The evolutionary history of vertebrate cranial placodes--I: cell type evolution.
Vertebrate cranial placodes
are crucial contributors to the vertebrate cranial sensory apparatus. Their evolutionary origin has attracted much attention from evolutionary and developmental biologists, yielding speculation and hypotheses concerning their putative homologues in other lineages and the developmental and genetic innovations that might have underlain their origin and diversification. In this article we first briefly review our current understanding of placode development and the cell types and structures they form. We next summarise previous hypotheses of placode evolution, discussing their strengths and caveats, before considering the evolutionary history of the various cell types that develop from placodes. In an accompanying review, we also further consider the evolution of ectodermal patterning. Drawing on data from vertebrates, tunicates, amphioxus, other bilaterians and cnidarians, we build these strands into a scenario of placode evolutionary history and of the genes, cells and developmental processes that underlie placode evolution and development.
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Vertebrate cranial placodes. (A) Chick embryo (modified from Streit, (2004)). (B) Xenopus embryo (modified from Schlosser and Northcutt, (2000)). (C) Developmental fates and derivative cell types of different cranial placodes (modified from Schlosser, (2005)).
A simplified phylogeny of the Bilateria, illustrating the relationships of the major taxonomic groups discussed in this paper. Historically, cranial placodes have been considered a vertebrate innovation and are marked as such on this figure. See Fig. 6 in Schlosser et al. (this issue) for a version of this phylogeny on which we have marked evolutionary origins for many of the characters (genes, regulatory interactions, cells and tissues) which together constitute cranial placodes.
Some of the protochordate structures hypothesised to be homologous to vertebrate placodes. (A) Head of an amphioxus (Branchiostoma floridae), showing lack of obvious cranial sensory organs. pb, pharyngeal basket. (B) Section through the head of an adult amphioxus showing Hatschek׳s pit (Hp) penetrating up from the pharynx and connecting with the neural tube (nt). n, notochord. (C) Amphioxus larva showing the pre-oral pit (pp). (D) Cleared specimen of the tunicate Clavelina lepadiformis, showing the oral (os) and atrial (as) siphons, and the position of the neural complex (nc). (E) Larval head of the tunicate Ciona intestinalis, showing the palps (p), the oral siphon primordium/neurohypophyseal duct (osp/nd) and an atrial siphon primoridum (asp). (F) Dissected neural complex from Ciona intestinalis stained with the Six3/6 orthologue CiSix3/6. The neural complex and ciliated funnel (cf) are marked
Proposition of possible scenarios for the evolution of placode derived cell types. (A) Representation of placode-related cell types believed to be present in the ancestor of chordates, and the cell types derived thereof in the descendant cephalochordates and vertebrates. (B) Novel cell types appear in two possible ways. In the process of segregation of function (top), a cell type becomes two sister cell types by splitting part of the transcriptomes between the two daughter cell types. In the process of gene network co-option (bottom), a new cell type originates by merging the transcriptome of two existing cell types. (C) Scenarios for the evolution of somatosensory (SSN: trigeminal/profundal, otic/lateral line) and viscerosensory (VSN: epibranchial) neurons from a putative ciliated primary sensory neuron. In the first scenario (upper pathway), the primary sensory cell splits into a secondary sensory cell and an afferent neuron by segregation of functions. Resulting neurons and sensory cells become three distinct sister cells corresponding to the trigeminal/profundal, otic/lateral line and epibranchial-derived neurons. Alternatively (lower pathway), three sister cell types first evolve as primary sensory neurons. Then the primary sensory cells split into secondary sensory cells and afferent neurons. Finally, in both scenarios, the secondary sensory cells of the trigeminal/profundal and epibranchial, but not otic/lateral line systems are lost.