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

  • 997
    views
  • 41
    downloads
  • 1
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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
  1. Further reading

Further reading

    1. Ecology
    2. Evolutionary Biology
    Chunxiao Li, Tao Deng ... Shiqi Wang
    Research Article

    The long-trunked elephantids underwent a significant evolutionary stage characterized by an exceptionally elongated mandible. The initial elongation and subsequent regression of the long mandible, along with its co-evolution with the trunk, present an intriguing issue that remains incompletely understood. Through comparative functional and eco-morphological investigations, as well as feeding preference analysis, we reconstructed the feeding behavior of major groups of longirostrine elephantiforms. In the Platybelodon clade, the rapid evolutionary changes observed in the narial region, strongly correlated with mandible and tusk characteristics, suggest a crucial evolutionary transition where feeding function shifted from the mandible to the trunk, allowing proboscideans to expand their niches to more open regions. This functional shift further resulted in elephantids relying solely on their trunks for feeding. Our research provides insights into how unique environmental pressures shape the extreme evolution of organs, particularly in large mammals that developed various peculiar adaptations during the late Cenozoic global cooling trends.

    1. Evolutionary Biology
    Tian Yue, Yongbo Guo ... Bing Su
    Research Article

    Compared with lowlander migrants, native Tibetans have a higher reproductive success at high altitude though the underlying mechanism remains unclear. Here, we compared the transcriptome and histology of full-term placentas between native Tibetans and Han migrants. We found that the placental trophoblast shows the largest expression divergence between Tibetans and Han, and Tibetans show decreased immune response and endoplasmic reticulum stress. Remarkably, we detected a sex-biased expression divergence, where the male-infant placentas show a greater between-population difference than the female-infant placentas. The umbilical cord plays a key role in the sex-biased expression divergence, which is associated with the higher birth weight of the male newborns of Tibetans. We also identified adaptive histological changes in the male-infant placentas of Tibetans, including larger umbilical artery wall and umbilical artery intima and media, and fewer syncytial knots. These findings provide valuable insights into the sex-biased adaptation of human populations, with significant implications for medical and genetic studies of human reproduction.