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Review
.2003 Mar;202(Pt 3):255-67.
doi: 10.1046/j.1469-7580.2003.00163.x.

Concordia discors: duality in the origin of the vertebrate tail

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Review

Concordia discors: duality in the origin of the vertebrate tail

Gregory R Handrigan. J Anat.2003 Mar.

Abstract

The vertebrate tail is an extension of the main body axis caudal to the anus. The developmental origin of this structure has been a source of debate amongst embryologists for the past century. Some view tail development as a continuation of the morphogenetic processes that shape the head and trunk (i.e. gastrulation). The alternative view, secondary development, holds that the tail forms in a manner similar to limb development, i.e. by secondary induction. Previous developmental studies have provided support for both views. Here I revisit these studies, describing caudal morphogenesis in select vertebrates, the associated genes and developmental defects, and, as a relevant aside, consider the developmental and evolutionary relationships of primary and secondary neurulation. I conclude that caudal development enlists both gastrulation and secondary induction, and that the application of recent high-resolution cell labelling technology may clarify how these discordant programmes interact in building the vertebrate tail.

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Figures

Fig. 1
Fig. 1
Vertebrate tail development by continued rostral development (model 1) and secondary development (model 2). According to model 1, morphogenetic movements (i.e. gastrulation) occurring within the head end of the embryo continue beyond the anus (dashed arrows). Secondary development (model 2), however, involves secondary inductive events, occurring within a tailbud comprising homogeneous mesenchyme, regulated by morphogenetic signals (white arrows) emanating from a thickened ectodermal ridge, i.e. VER. Secondary structures (neural tube, notochord, somites) arise directly from mesenchyme without germ layers as an intermediate. Whole arrows denote the progress of development.
Fig. 2
Fig. 2
A phylogeny of the chordates (based on Zardoya & Meyer, 1996; Mallatt & Sullivan, 1998; Cotton & Page, 2002) with data for primary and secondary neurulation (see text for cited literature). Primary neurulation, as seen in ascidians and the majority of vertebrate taxa, probably represents the ancestral chordate condition. Neural plate folding in amphioxus, a process consistent with primary neurulation, has been uncoupled from epidermal overgrowth. This event is thought to be related to the advent of the neural crest in craniates (Holland et al. 1996). Secondary neurulation, the derived condition in vertebrates, is presumed to have arisen by parallel substitution events in lampreys, neopterygian fishes, dipnoans (Lepidosiren andProtopterus with the exception ofCeratodus), and possibly tetrapods. Taxa for which data are missing are indicated in grey. Branches marked with asterisks are unresolved and have been represented as trichotomies.
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