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Development

Somite number and vertebrate evolution

Profile image of James HankenJames Hanken

1998, Development

https://doi.org/10.1242/DEV.125.2.151
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Abstract

Variation in segment number is an important but neglected feature of vertebrate evolution. Some vertebrates have as few as six trunk vertebrae, while others have hundreds. We examine this phenomenon in relation to recent models of evolution and development. Surprisingly, differences in vertebral number are foreshadowed by different somite counts at the tailbud stage, thought to be a highly conserved (phylotypic) stage. Somite number therefore violates the ‘developmental hourglass’ model. We argue that this is because somitogenesis shows uncoupling or dissociation from the conserved positional field encoded by genes of the zootype. Several other systems show this kind of dissociation, including limbs and feathers. Bmp-7 expression patterns demonstrate dissociation in the chick pharyngeal arches. This makes it difficult to recognise a common stage of pharyngeal development or ‘pharyngula’ in all species. Rhombomere number is more stable during evolution than somite number, possibly be...

Figures (7)
Fig. 3. Comparison of somitogenesis in a short-bodied species with few somites, and a long-bodied species with a high somite count. Illustrations based on Tavolga (1949); and Sammouri et al. (1990) with permission. (A,B) Platyfish, Xiphophorus maculatus. (A) eurula stage with otic placodes and optic outgrowths. No somites have developed. Dorsal view. (B) Tailbud stage. Only 13 somites have segregated. Lateral view. (C,D) Caecilian amphibian Typhlonectes compressicaudus. (C) Neurula stage. In contrast to the platyfish, many somites have already appeared. Dorsal view. (D) By the tailbud stage, the body of Typhlonectes has become highly elongate and has over 50 somites, several times more than in the platyfish. Lateral view.
Fig. 3. Comparison of somitogenesis in a short-bodied species with few somites, and a long-bodied species with a high somite count. Illustrations based on Tavolga (1949); and Sammouri et al. (1990) with permission. (A,B) Platyfish, Xiphophorus maculatus. (A) eurula stage with otic placodes and optic outgrowths. No somites have developed. Dorsal view. (B) Tailbud stage. Only 13 somites have segregated. Lateral view. (C,D) Caecilian amphibian Typhlonectes compressicaudus. (C) Neurula stage. In contrast to the platyfish, many somites have already appeared. Dorsal view. (D) By the tailbud stage, the body of Typhlonectes has become highly elongate and has over 50 somites, several times more than in the platyfish. Lateral view.
Fig. 4. Somite number in evolution and development. (A) The ‘developmental hourglass’ predicts that species show convergence towards, and divergence from, a conserved phylotypic (tailbud) stage. This model cannot account for differences in somite number, which show continuous divergence before, during and after the phylotypic stage. (B) A better representation of evolutionary changes in somitogenesis in this case. Based on a comparison between the platyfish and the caecilian Typhlonectes compressicaudus (see Fig 3). See also Richardson et al. (1997) for details of variations in somite number at the phylotypic stage.
Fig. 4. Somite number in evolution and development. (A) The ‘developmental hourglass’ predicts that species show convergence towards, and divergence from, a conserved phylotypic (tailbud) stage. This model cannot account for differences in somite number, which show continuous divergence before, during and after the phylotypic stage. (B) A better representation of evolutionary changes in somitogenesis in this case. Based on a comparison between the platyfish and the caecilian Typhlonectes compressicaudus (see Fig 3). See also Richardson et al. (1997) for details of variations in somite number at the phylotypic stage.
paraxial mesoderm of the embryo coincides approximately with the axial level of the forelimb or pectoral fin, even though this lies opposite different numbered somites in different species (numbered arrows). Forelimb or pectoral fin bud shown in red.
paraxial mesoderm of the embryo coincides approximately with the axial level of the forelimb or pectoral fin, even though this lies opposite different numbered somites in different species (numbered arrows). Forelimb or pectoral fin bud shown in red.
Fig. 6. Reaggregate limbs provide experimental evidence of dissociation between repeating patterns and the Hox genes, which encode positional value. Based on Hardy et al. (1995). (A) The normal chick leg bud (left) gives rise to a polarised digit pattern (right). Anterior is to the top, distal is to the right. Hoxd-13 (Purple) is expressed near the posterior margin at early stages. (B) Reaggregate limb bud (left). Because the polarising region has been scrambled, Hoxd-13 expression is not polarised. A pattern of digits is still generated, despite the lack of an AP gradient of positional information.
Fig. 6. Reaggregate limbs provide experimental evidence of dissociation between repeating patterns and the Hox genes, which encode positional value. Based on Hardy et al. (1995). (A) The normal chick leg bud (left) gives rise to a polarised digit pattern (right). Anterior is to the top, distal is to the right. Hoxd-13 (Purple) is expressed near the posterior margin at early stages. (B) Reaggregate limb bud (left). Because the polarising region has been scrambled, Hoxd-13 expression is not polarised. A pattern of digits is still generated, despite the lack of an AP gradient of positional information.

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Proceedings of the Royal Society B: Biological Sciences, 2003

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Major shifts in the evolution of somitogenesis: The reptile Anolis carolinensis represents a fourth type of segmentation clock among vertebrates
Dale Denardo

Developmental Biology, 2011

The axial skeleton is a defining feature of vertebrates and is patterned during somitogenesis. Cyclically expressed members of the notch and other signaling pathways, described as the 'segmentation clock', regulate the formation of somite boundaries. Comparisons among vertebrate model systems have revealed fundamental shifts in the regulation of expression among critical genes in the notch pathway. However, insights into the evolution of these expression differences have been limited by the lack of information from nonavian reptiles. We analyzed the segmentation clock of the first Lepidosaurian reptile sequenced, the green anole lizard, Anolis carolinensis, for comparison with avian and mammalian models. Using genomic sequence, RNA-Seq transcriptomic data, and in situ hybridization analysis of somite-stage embryos, we carried out comparative analyses of key genes and found that the anole segmentation clock displays features common to both amniote and anamniote vertebrates. Shared features with anamniotes, represented by Xenopus laevis and Danio rerio, include an absence of lunatic fringe (lfng) expression within the presomitic mesoderm (PSM), a hes6a gradient in the PSM not observed in the chicken or mouse, and EGF repeat structure of the divergent notch ligand, dll3. The anole and mouse share cycling expression of dll1 ligand in the PSM. To gain insight from an Archosaurian reptile, we analysed LFNG and DLL1 expressions in the American alligator. LFNG expression was absent in the alligator PSM, like the anole but unlike the chicken. In contrast, DLL1 expression does not cycle in the PSM of the alligator, similar to the chicken but unlike the anole. Thus, our analysis yields novel insights into features of the segmentation clock that are evolutionarily basal to amniotes versus those that are specific to mammals, Lepidosaurian reptiles, or Archosaurian reptiles.

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

Anatomy and Embryology, 1997

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.

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The developmental fate of the rostral/caudal half of a somite for vertebra and rib formation: experimental confirmation of the resegmentation theory using chick-quail chimeras
Hirohiko Aoyama

Mechanisms of Development, 2000

To determine whether resegmentation of somites forms the axial skeleton, we traced the development of the rostral and the caudal half of a somite during skeletogenesis in chick-quail chimeras by replacing the rostral or caudal half of a newly formed chick somite with that of a quail somite. The rostral half-somite transplant formed the caudal half of the vertebral body, the entire spinous process and the distal rib, while the caudal half-somite transplant formed the rostral half of vertebral body, the rostral half of spinous process, the vertebral arch, the transverse process and the entire rib. These ®ndings con®rm the resegmentation theory except the spinous process and the distal rib.

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Serial Homology and the Evolution of Mammalian Limb Covariation Structure
Nathan Young

Evolution, 2005

The tetrapod forelimb and hindlimb are serially homologous structures that share a broad range of devel- opmental pathways responsible for their patterning and outgrowth. Covariation between limbs, which can introduce constraints on the production of variation, is related to the duplication of these developmental factors. Despite this constraint, there is remarkable diversity in limb morphology, with a variety of functional relationships between and within forelimb and hindlimb elements. Here we assess a hierarchical model of limb covariation structure based on shared developmental factors. We also test whether selection for morphologically divergent forelimbs or hindlimbs is associated with reduced covariation between limbs. Our sample includes primates, murines, a carnivoran, and a chiropteran that exhibit varying degrees of forelimb and hindlimb specialization, limb size divergence, and/or phy- logenetic relatedness. We analyze the pattern and significance of between-limb morphological covariation with linear distance data collected using standard morphometric techniques and analyzed by matrix correlations, eigenanalysis, and partial correlations. Results support a common limb covariation structure across these taxa and reduced covariation between limbs in nonquadruped species. This result indicates that diversity in limb morphology has evolved without signficant modifications to a common covariation structure but that the higher degree of functional limb divergence in bats and, to some extent, gibbons is associated with weaker integration between limbs. This result supports the hypothesis that limb divergence, particularly selection for increased functional specialization, involves the reduction of developmental factors common to both limbs, thereby reducing covariation.

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