The turtles, or Testudines (Order Testudines, Class Reptilia) are informally divided into two categories, depending on whether the animal has an aquatic or terrestrial lifestyle. The term "turtle" is usually restricted to aquatic forms, while those that live on land are generally called tortoises.
All extant Testudines fall into two clades, the Cryptodira and the Pleurodira. The difference between these two groups is a function of the manner in which the turtles retract their head into their shell: the cryptodires, or hidden-necked turtles, pull their heads directly in, while the pleurodires, or side-necked turtles, move their head to one side as they retract it.
All members of the turtle total group are characterized by having a complete shell, which is a composite structure comprising the bony plates of the (dorsal) carapace and (ventral) plastron (Joyce et al, 2021). This characteristic is an apomorphy rather than a synapomorphy, because there is no knowledge of any ancestor that shared that feature.
The origin of the turtles remains an unresolved question. The following diagram illustrates the four main phylogenetic hypotheses:
All extant Testudines fall into two clades, the Cryptodira and the Pleurodira. The difference between these two groups is a function of the manner in which the turtles retract their head into their shell: the cryptodires, or hidden-necked turtles, pull their heads directly in, while the pleurodires, or side-necked turtles, move their head to one side as they retract it.
All members of the turtle total group are characterized by having a complete shell, which is a composite structure comprising the bony plates of the (dorsal) carapace and (ventral) plastron (Joyce et al, 2021). This characteristic is an apomorphy rather than a synapomorphy, because there is no knowledge of any ancestor that shared that feature.
The origin of the turtles remains an unresolved question. The following diagram illustrates the four main phylogenetic hypotheses:
Figure 1. Alternative phylogenetic placements of turtles
The four hypotheses, indicated by the red numbers above, are summarized by Lyson & Bever (2020) as follows:
Many phylogenetic trees have been published for the turtle stem group, and recent versions (e.g. Joyce et al, 2016; Sterli et al, 2021) are generally consistent with one another. The following phylogenetic time tree is based on Sterli et al (2021):
- Turtles are well outside the crown-Diapsida and the crown-Sauria. This hypothesis is based on early analysis (1988 – 1997) derived solely from morphological data.
- Turtles are within the crown-Sauria and form a sister group to the Lepidosauria. This view, also using only morphology, is based on more recent work and is still considered valid by some researchers, (e.g. Schoch and Sues, 2015).
- A third morphology-based hypothesis indicates that turtles are within crown-Diapsida but derive from the stem line of the Sauria (e.g. Bever et al, 2015).
- This hypothesis, based on molecular data, is that turtles are a sister group to the Archosauria within a clade named the Archelosauria (e.g. Crawford et al, 2015).
Many phylogenetic trees have been published for the turtle stem group, and recent versions (e.g. Joyce et al, 2016; Sterli et al, 2021) are generally consistent with one another. The following phylogenetic time tree is based on Sterli et al (2021):
Figure 2. Phylogenetic time tree of the stem-Testudines
The earliest known stem turtle is Odontochelys semitestacea, described from the Late Triassic (Carnian) Wayao Member of the Falang Formation at Guanling, Guizhou Province, southwestern China (Li et al, 2008; Joyce et al, 2016). This species is illustrated below, together with other species for which images are available in the public domain (click on image for larger view):
Names in red indicate that the fossil is younger than the oldest known crown-group fossil.
Figure 3. Images of stem-group turtles
The above images are ordered from most basal to most crownward, but the fossils shown do not demonstrate the process whereby a complete turtle shell developed. This issue is discussed comprehensively by Schoch and Sues (2020); the evolutionary process is illustrated in their Figure 3, reproduced below:
Figure 4. Morphological transformation series for Triassic stem-turtles leading up to the presence of a fully developed bony shell in
Proganochelys.
Proganochelys.
Note that Figure 4 includes Pappochelys rosinae, which has been interpreted as a stem turtle (e.g. Schoch and Sues, 2015), but Szczygielski (2017) documented the instability of phylogenetic trees that include that species while the analysis of Lichtig and Lucas (2021) interpreted Pappochelys as a possible member of the Sauropterygia, a huge group of extinct marine reptiles, including the plesiosaurs, whose phylogenetic placement remains unclear (Voeten et al, 2018). The sauropterygians have been placed as sister to a clad comprising the lepidosaurs and the archosaurs (Neenan et al, 2013; Wang et al, 2019), sister to the turtles (Jiang et al, 2018) or sister to the lepidosaurs (Lichtig and Lucas, 2021).
Returning to the fossil images shown above, it can be seen that one branch of the stem group, the family Meiolaniidae, have armoured heads (see images of Niolamia argentina, Ninjemys oweni and Meiolania platyceps above), but this group appears to represent an evolutionary dead end.
Note that most of the stem species have their names in red, which indicates that they post-date the appearance of the crown group; these represent branches of the stem line that continued to evolve after the crown-group had appeared.
The oldest known crown-group testudine fossil is the stem pleurodire Caribemys oxfordiensis, described from the Late Jurassic (Middle - Late Oxfordian) Jagua Vieja Memberof the Jagua Formation at the Viñales locality, Pinar del Río Province, Cuba (De la Fuente and Iturralde-Vinent, 2001; Joyce et al, 2016). No images of this species are available in the public domain.
The turtle stem line includes a ghost lineage (shown as a blue bar in Figure 2), because the oldest known total-group archosaur (of Middle to Late Permian age; see page on the Archosauria) is at least 20 million years older than the stem-group turtles, which are of Late Triassic and younger age. Given that the two stem groups must have appeared at the same time, the turtle stem-group transition must also have begun in the Middle to Late Permian. This implies a stem-to-crown transition of at least 93 million years.
Returning to the fossil images shown above, it can be seen that one branch of the stem group, the family Meiolaniidae, have armoured heads (see images of Niolamia argentina, Ninjemys oweni and Meiolania platyceps above), but this group appears to represent an evolutionary dead end.
Note that most of the stem species have their names in red, which indicates that they post-date the appearance of the crown group; these represent branches of the stem line that continued to evolve after the crown-group had appeared.
The oldest known crown-group testudine fossil is the stem pleurodire Caribemys oxfordiensis, described from the Late Jurassic (Middle - Late Oxfordian) Jagua Vieja Memberof the Jagua Formation at the Viñales locality, Pinar del Río Province, Cuba (De la Fuente and Iturralde-Vinent, 2001; Joyce et al, 2016). No images of this species are available in the public domain.
The turtle stem line includes a ghost lineage (shown as a blue bar in Figure 2), because the oldest known total-group archosaur (of Middle to Late Permian age; see page on the Archosauria) is at least 20 million years older than the stem-group turtles, which are of Late Triassic and younger age. Given that the two stem groups must have appeared at the same time, the turtle stem-group transition must also have begun in the Middle to Late Permian. This implies a stem-to-crown transition of at least 93 million years.
References
Benton, M. J. (2015). Vertebrate Palaeontology - Fourth edition. John Wiley & Sons, 468 pages.
Bever, G. S., Lyson, T. R., Field, D. J., & Bhullar, B. A. S. (2015). Evolutionary origin of the turtle skull. Nature, 525(7568), 239-242.
Crawford, N. G., Parham, J. F., Sellas, A. B., Faircloth, B. C., Glenn, T. C., Papenfuss, T. J., ... & Simison, W. B. (2015). A phylogenomic analysis of turtles. Molecular phylogenetics and evolution, 83, 250-257.
De la Fuente, M. S., & Iturralde-Vinent, M. (2001). A new pleurodiran turtle from the Jagua Formation (Oxfordian) of western Cuba. Journal of Paleontology, 75(4), 860-869.
Jiang, D. Y., Lin, W. B., Rieppel, O., Motani, R., & Sun, Z. Y. (2018). A new Anisian (Middle Triassic) eosauropterygian (Reptilia, Sauropterygia) from Panzhou, Guizhou Province, China. Journal of Vertebrate Paleontology, 38(4), 1-9.
Joyce, W. G., Rabi, M., Clark, J. M., & Xu, X. (2016). A toothed turtle from the Late Jurassic of China and the global biogeographic history of turtles. BMC Evolutionary Biology, 16(1), 1-29.
Joyce, W. G., Anquetin, J., Cadena, E. A., Claude, J., Danilov, I. G., Evers, S. W., ... & Parham, J. F. (2021). A nomenclature for fossil and living turtles using phylogenetically defined clade names. Swiss Journal of Palaeontology, 140(1), 1-45.
Li, C., Wu, X. C., Rieppel, O., Wang, L. T., & Zhao, L. J. (2008). An ancestral turtle from the Late Triassic of southwestern China. Nature, 456(7221), 497-501.
Lichtig, A. J., & Lucas, S. G. (2021). Chinlechelys from the Upper Triassic of New Mexico, USA, and the origin of turtles. Palaeontologia Electronica, 24(1):a13. https://doi.org/10.26879/886
Lyson, T. R., & Bever, G. S. (2020). Origin and evolution of the turtle body plan. Annual Review of Ecology, Evolution, and Systematics, 51, 143-166.
Neenan, J. M., Klein, N., & Scheyer, T. M. (2013). European origin of placodont marine reptiles and the evolution of crushing dentition in Placodontia. Nature Communications, 4(1), 1-8.
Schoch, R. R., & Sues, H. D. (2015). A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature, 523(7562), 584-587.
Schoch, R. R., & Sues, H. D. (2020). The origin of the turtle body plan: evidence from fossils and embryos. Palaeontology, 63(3), 375-393.
Sterli, J., Martinez, R. N., Cerda, I. A., & Apaldetti, C. (2021). Appearances can be deceptive: bizarre shell microanatomy and histology in a new Triassic turtle (Testudinata) from Argentina at the dawn of turtles. Papers in Palaeontology, 7(2), 1097-1132.
Szczygielski, T. (2017). Homeotic shift at the dawn of the turtle evolution. Royal Society open science, 4(4), 160933.
Voeten, D. F., Reich, T., Araujo, R., & Scheyer, T. M. (2018). Synchrotron microtomography of a Nothosaurus marchicus skull informs on nothosaurian physiology and neurosensory adaptations in early Sauropterygia. PLoS One, 13(1), e0188509.
Wang, W., Li, C., & Wu, X. C. (2019). An adult specimen of Sinocyamodus xinpuensis (Sauropterygia: Placodontia) from Guanling, Guizhou, China. Zoological Journal of the Linnean Society, 185(3), 910-924.
Bever, G. S., Lyson, T. R., Field, D. J., & Bhullar, B. A. S. (2015). Evolutionary origin of the turtle skull. Nature, 525(7568), 239-242.
Crawford, N. G., Parham, J. F., Sellas, A. B., Faircloth, B. C., Glenn, T. C., Papenfuss, T. J., ... & Simison, W. B. (2015). A phylogenomic analysis of turtles. Molecular phylogenetics and evolution, 83, 250-257.
De la Fuente, M. S., & Iturralde-Vinent, M. (2001). A new pleurodiran turtle from the Jagua Formation (Oxfordian) of western Cuba. Journal of Paleontology, 75(4), 860-869.
Jiang, D. Y., Lin, W. B., Rieppel, O., Motani, R., & Sun, Z. Y. (2018). A new Anisian (Middle Triassic) eosauropterygian (Reptilia, Sauropterygia) from Panzhou, Guizhou Province, China. Journal of Vertebrate Paleontology, 38(4), 1-9.
Joyce, W. G., Rabi, M., Clark, J. M., & Xu, X. (2016). A toothed turtle from the Late Jurassic of China and the global biogeographic history of turtles. BMC Evolutionary Biology, 16(1), 1-29.
Joyce, W. G., Anquetin, J., Cadena, E. A., Claude, J., Danilov, I. G., Evers, S. W., ... & Parham, J. F. (2021). A nomenclature for fossil and living turtles using phylogenetically defined clade names. Swiss Journal of Palaeontology, 140(1), 1-45.
Li, C., Wu, X. C., Rieppel, O., Wang, L. T., & Zhao, L. J. (2008). An ancestral turtle from the Late Triassic of southwestern China. Nature, 456(7221), 497-501.
Lichtig, A. J., & Lucas, S. G. (2021). Chinlechelys from the Upper Triassic of New Mexico, USA, and the origin of turtles. Palaeontologia Electronica, 24(1):a13. https://doi.org/10.26879/886
Lyson, T. R., & Bever, G. S. (2020). Origin and evolution of the turtle body plan. Annual Review of Ecology, Evolution, and Systematics, 51, 143-166.
Neenan, J. M., Klein, N., & Scheyer, T. M. (2013). European origin of placodont marine reptiles and the evolution of crushing dentition in Placodontia. Nature Communications, 4(1), 1-8.
Schoch, R. R., & Sues, H. D. (2015). A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature, 523(7562), 584-587.
Schoch, R. R., & Sues, H. D. (2020). The origin of the turtle body plan: evidence from fossils and embryos. Palaeontology, 63(3), 375-393.
Sterli, J., Martinez, R. N., Cerda, I. A., & Apaldetti, C. (2021). Appearances can be deceptive: bizarre shell microanatomy and histology in a new Triassic turtle (Testudinata) from Argentina at the dawn of turtles. Papers in Palaeontology, 7(2), 1097-1132.
Szczygielski, T. (2017). Homeotic shift at the dawn of the turtle evolution. Royal Society open science, 4(4), 160933.
Voeten, D. F., Reich, T., Araujo, R., & Scheyer, T. M. (2018). Synchrotron microtomography of a Nothosaurus marchicus skull informs on nothosaurian physiology and neurosensory adaptations in early Sauropterygia. PLoS One, 13(1), e0188509.
Wang, W., Li, C., & Wu, X. C. (2019). An adult specimen of Sinocyamodus xinpuensis (Sauropterygia: Placodontia) from Guanling, Guizhou, China. Zoological Journal of the Linnean Society, 185(3), 910-924.
Image credits – Stem-Testudines
- Header (Oldham's leaf turtle, Cyclemys oldhamii): Thai National Parks, under the Creative Commons Attribution-Share-Alike Licence 3.0.
- Figure 3 (Odontochelys semitestacea, fossil): Jonathan Chen, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Figure 3 (Odontochelys semitestacea, life restoration): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Figure 3 (Proganochelys quenstedti, fossil): Photographed by Bob James (owner of website) at American Museum of Natural History, New York, May 2024.
- Figure 3 (Proganochelys quenstedti, life restoration): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Figure 3 (skull of Kayentachelys aprix): Sterli, J. and Joyce, W.G., CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Figure 3 (Kayentachelys aprix, life restoration): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Figure 3 (Kallokibotion bajazidi): Gyik Toma (Tommy the paleobear) from Romania, CC BY 2.0 <https://creativecommons.org/licenses/by/2.0>, via Wikimedia Commons
- Figure 3 (Naomichelys sp.): Jonathan Chen, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Figure 3 (Helochelydra nopcsai): DaCaTaraptor, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Figure 3 (Niolamia argentina): Heinrich Harder (1858-1935), Public domain, via Wikimedia Commons
- Figure 3 (Pleurosternon bullockii): Open Access article Evers, S. W., Rollot, Y., & Joyce, W. G. (2020). Cranial osteology of the Early Cretaceous turtle Pleurosternon bullockii (Paracryptodira: pleurosternidae). PeerJ, 8, e9454.
- Figure 3 (Ninjemys oweni): Ghedoghedo, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Figure 3 (Meiolania platyceps, fossil): Fanny Schertzer, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Figure 3 (Meiolania platyceps, life restoration): WSnyder, Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 License
- Figure 3 (Dorsetochelys delairi): British Geological Survey, under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.
- Figure 3 (Sichuanchelys palatodentata): Joyce et al., CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Figure 3 (Glyptops ornatus): Marsh, Public domain, via Wikimedia Commons
- Figure 3 (Dinochelys whitei): James St. John, CC BY 2.0 <https://creativecommons.org/licenses/by/2.0>, via Wikimedia Commons
- Figure 3 (Neurankylus utahensis): Bureau of Land Management - Utah, Public domain, via Wikimedia Commons
- Figure 3 (Chisternon undatum): Claire Houck from New York City, USA, CC BY-SA 2.0 <https://creativecommons.org/licenses/by-sa/2.0>, via Wikimedia Commons
- Figure 3 (Baena arenosa): Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons