There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development

Abstract

Embryos of different species of vertebrate share a common organisation and often look similar. Adult differences among species become more apparent through divergence at later stages. Some authors have suggested that members of most or all vertebrate clades pass through a virtually identical, conserved stage. This idea was promoted by Haeckel, and has recently been revived in the context of claims regarding the universality of developmental mechanisms. Thus embryonic resemblance at the tailbud stage has been linked with a conserved pattern of developmental gene expression - the zootype. Haeckel's drawings of the external morphology of various vertebrates remain the most comprehensive comparative data purporting to show a conserved stage. However, their accuracy has been questioned and only a narrow range of species was illustrated. In view of the current widespread interest in evolutionary developmental biology, and especially in the conservation of developmental mechanisms, re-examination of the extent of variation in vertebrate embryos is long overdue. We present here the first review of the external morphology of tailbud embryos, illustrated with original specimens from a wide range of vertebrate groups. We find that embryos at the tailbud stage - thought to correspond to a conserved stage - show variations in form due to allometry, heterochrony, and differences in body plan and somite number. These variations foreshadow important differences in adult body form. Contrary to recent claims that all vertebrate embryos pass through a stage when they are the same size, we find a greater than 10-fold variation in greatest length at the tailbud stage. Our survey seriously undermines the credibility of Haeckel's drawings, which depict not a conserved stage for vertebrates, but a stylised amniote embryo. In fact, the taxonomic level of greatest resemblance among vertebrate embryos is below the subphylum. The wide variation in morphology among vertebrate embryos is difficult to reconcile with the idea of a phyogenetically-conserved tailbud stage, and suggests that at least some developmental mechanisms are not highly constrained by the zootype. Our study also highlights the dangers of drawing general conclusions about vertebrate development from studies of gene expression in a small number of laboratory species.

Ghrelin-producing epsilon cells in the developing and adult human pancreas

“…1). Later (weeks [17][18][19][20], epsilon cells started to aggregate into clusters, but unlike insulinand glucagon-reactive cells, which are predominantly localised to clusters at this age (ESM Fig. 3, ESM Fig.…”

“…Like the mouse pancreas, the human pancreas develops from two endodermal diverticula, the dorsal and ventral [1], which fuse at about 56 days of development post coitum [18]. However, the morphogenesis of the endocrine tissue is unlikely to be comparable between species, given the differences in gestation and the larger relative volume of the human pancreas [19]. Extrapolation of rodent-derived knowledge of epsilon cells and pancreatic development to humans is therefore problematic.…”

Brain expansion and comparative prenatal ontogeny of the non-hominoid primate cranial base

“…Perhaps the initial conserved stage of basicranial morphogenesis as posited by Jeffery and Spoor (2002) is a misconception. Indeed, studies show that contrary to the influential drawings made by Haeckel (1891), morphological differences between adult species can be traced back to the early embryonic stages of life (Richardson et al, 1997;Bininda-Emonds et al, 2003). Furthermore, Sperber (2001) notes an acute angulation of the human midline basicranium at around 4 weeks gestation.…”

A Cell Cycle Model for Somitogenesis: Mathematical Formulation and Numerical Simulation

“…However, it is worth noting that the anomalies in zebra"sh appear at exactly twice the frequency predicted by the cell cycle model. Together with the "nding that this group of teleosts has undergone an additional round of genome duplication (see Richardson et al, 1997), one possible scenario is that two separate genes (and/or two separate clocks linked to the cell cycle, but half-a-cycle out of phase with one another) regulate somitogenesis in these animals. Supporting this suggestion is the "nding that another member of the hairy-enhancer of split family, her-1, has been characterized as having an expression pattern in every other somite (MuK ller et al, 1996), unlike any gene thus far described in other vertebrates.…”