Morphology: Too hip for two sacral vertebrae

A complex pelvic morphology has been discovered in the fossils of one of the largest crocodylians.
  1. Michelle R Stocker  Is a corresponding author
  1. Virginia Tech, United States

The properties of vertebrae – the bones that make up the backbone – have a crucial influence on the way that mammals, birds, fishes and many other vertebrate species move. Some vertebrates have vertebrae that are rather charismatic in terms of size, shape or number. For example, all mammals possess seven vertebrae within their necks, whether they are a giraffe or a mouse, and the length of these vertebrae depends on the length of the neck.

Reptiles typically have two vertebrae in their sacrum, which is near the pelvis (Hoffstetter and Gasc, 1969). Having two sacral vertebrae is characteristic of the Archosauromorpha, a group that includes crocodylians (large, predatory, aquatic and semiaquatic reptiles) and their extinct close relatives (Nesbitt, 2011; Griffin et al., 2017). However, birds and their close relatives among non-avian theropods (dinosaurs with hollow bones and three toes) deviate from this trend of having two vertebrae in the sacrum. Many birds have at least 12 sacral vertebrae, and swans have 24 (Turner et al., 2012)!

Studies of growth in living species, like the chicken, show that the ordering of the body during development – and the number of vertebrae formed – is controlled by a group of genes called the Hox genes. These genes have recently been shown to control patterning in other archosauromorphs, including crocodylians (e.g. Böhmer et al., 2015).

But this is all in living species, what about fossils? It is known, for example, that some early theropod fossils (like those of Tyrannosaurus or Velociraptor) exhibit more than two sacral vertebrae (Turner et al., 2012). Exploring the vertebrae of fossils helps to fill in the gaps in our understanding of morphology, and helps explain why modern groups look the way they do and how extinct members of those groups organized their body plans.

Now, in eLife, Torsten Scheyer of the University of Zurich and co-workers in Switzerland, the United Kingdom, Italy, Spain and Venezuela report on a crocodylian fossil that has more than two sacral vertebrae (Scheyer et al., 2019). The extinct Purussaurus mirandai, one of the largest known crocodylians, is found fossilized in rocks in northern South America that are between 5 and 13 million years old, and is related to crocodylians alive today. This giant caiman is known for its very large skull, but Scheyer et al. have now described all the other bones known to be associated with the species. As part of that description, they examined the sacral vertebrae and found the first non-pathological case of a crocodylian with more than two vertebrae in their sacrum (Figure 1).

Fossilized sacral vertebrae of Purussaurus mirandai.

Scheyer et al. have examined the skeleton of the crocodylian P. mirandai. All other crocodylians examined to date only have two vertebrae in their sacrum, making P. mirandai the first reported case of a crocodylian with three sacral vertebrae. This is likely due to a change in the expression of the Hox genes in this species. Indicated as prz in the image, the prezygagophysis connects each vertebra with the anterior one in the spine.

How did the number of vertebrae increase? As the skeleton grows, three types of changes are possible: a vertebra could be added from the tail (i.e., the ‘caudal’ vertebrae), creating a caudosacral; a vertebra could be inserted between the original two; or a vertebra could be added from the front, creating a dorsosacral. Scheyer et al. show that P. mirandai has the two original sacral vertebrae as well as a dorsosacral, similar to some extinct crocodylian-like animals called phytosaurs (Griffin et al., 2017).

But why would a species add vertebrae? An expanded sacrum might give vertebrates increased stability. This is important when a species increases in size, or when it becomes bipedal (and has to be able to balance while standing on two legs). Scheyer et al. looked at other parts of the skeleton to answer why P. mirandai had an extra vertebra, examining the shoulder girdle. In these specimens, the shoulder girdle is oriented more vertically than in other crocodylians with just two sacral vertebrae. This, along with the expanded pelvis, is evidence for weight being supported by the limbs rather than the trunk, hinting at the species becoming more upright. Crocodylians also have massive, muscular tails, which add to the weight that has to be supported and also changes the center of mass (Molnar et al., 2014).

These newly examined specimens of P. mirandai show that crocodylians have the ability to expand the number of sacral vertebrae, suggesting a change in the pattern of Hox gene expression in this species. There is evidence that other non-dinosaurian archosauromorphs, such as phytosaurs, expanded their sacral vertebrae, too, despite having evolved separately (Griffin et al., 2017). However, a sacrum with more than two sacral vertebrae has evolved multiple times independently, especially in animals from the Triassic Period (~250–200 million years ago). The confirmation that crocodylians can have more than two sacral vertebrae rewrites what was thought of as possible for this group of animals, adding an interesting new layer of developmental and morphological flexibility.

References

  1. Book
    1. Hoffstetter R
    2. Gasc J-P
    (1969)
    Vertebrae and ribs of modern reptiles
    In: Gans C, Bellairs A. D. A, Parsons T. S, editors. Biology of the Reptilia. Volume 1. Morphology A. London: Academic Press. pp. 201–310.

Article and author information

Author details

  1. Michelle R Stocker

    Michelle R Stocker is in the Department of Geosciences, Virginia Tech, Blacksburg, United States

    For correspondence
    stockerm@vt.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6473-8691

Publication history

  1. Version of Record published: December 19, 2019 (version 1)

Copyright

© 2019, Stocker

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 692
    Page views
  • 35
    Downloads
  • 1
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Michelle R Stocker
(2019)
Morphology: Too hip for two sacral vertebrae
eLife 8:e53399.
https://doi.org/10.7554/eLife.53399

Further reading

    1. Ecology
    2. Evolutionary Biology
    Animesh Gupta et al.
    Research Article

    During the struggle for survival, populations occasionally evolve new functions that give them access to untapped ecological opportunities. Theory suggests that coevolution between species can promote the evolution of such innovations by deforming fitness landscapes in ways that open new adaptive pathways. We directly tested this idea by using high-throughput gene editing-phenotyping technology (MAGE-Seq) to measure the fitness landscape of a virus, bacteriophage λ, as it coevolved with its host, the bacterium Escherichia coli. An analysis of the empirical fitness landscape revealed mutation-by-mutation-by-host-genotype interactions that demonstrate coevolution modified the contours of λ’s landscape. Computer simulations of λ’s evolution on a static versus shifting fitness landscape showed that the changes in contours increased λ’s chances of evolving the ability to use a new host receptor. By coupling sequencing and pairwise competition experiments, we demonstrated that the first mutation λ evolved en route to the innovation would only evolve in the presence of the ancestral host, whereas later steps in λ’s evolution required the shift to a resistant host. When time-shift replays of the coevolution experiment were run where host evolution was artificially accelerated, λ did not innovate to use the new receptor. This study provides direct evidence for the role of coevolution in driving evolutionary novelty and provides a quantitative framework for predicting evolution in coevolving ecological communities.

    1. Developmental Biology
    2. Evolutionary Biology
    Alexandre P Thiery et al.
    Research Article Updated

    Development of tooth shape is regulated by the enamel knot signalling centre, at least in mammals. Fgf signalling regulates differential proliferation between the enamel knot and adjacent dental epithelia during tooth development, leading to formation of the dental cusp. The presence of an enamel knot in non-mammalian vertebrates is debated given differences in signalling. Here, we show the conservation and restriction of fgf3, fgf10, and shh to the sites of future dental cusps in the shark (Scyliorhinus canicula), whilst also highlighting striking differences between the shark and mouse. We reveal shifts in tooth size, shape, and cusp number following small molecule perturbations of canonical Wnt signalling. Resulting tooth phenotypes mirror observed effects in mammals, where canonical Wnt has been implicated as an upstream regulator of enamel knot signalling. In silico modelling of shark dental morphogenesis demonstrates how subtle changes in activatory and inhibitory signals can alter tooth shape, resembling developmental phenotypes and cusp shapes observed following experimental Wnt perturbation. Our results support the functional conservation of an enamel knot-like signalling centre throughout vertebrates and suggest that varied tooth types from sharks to mammals follow a similar developmental bauplan. Lineage-specific differences in signalling are not sufficient in refuting homology of this signalling centre, which is likely older than teeth themselves.