Complete

Phylogeny and Classification of Amniotes

Michel Laurin and Jacques A. Gauthier

The phylogeny of early groups of amniotes has been in a state of flux in the last few years, but the first phylogeny based on a data matrix was published in the eighties (Gauthier et al., 1988). The origins of mammals and saurians from early synapsids and early diapsids, respectively, has been relatively non-controversial, but the origin of turtles has been problematic. The most widespread view, at least until the last few years, was that the closest extinct relatives of turtles were the captorhinids (Gaffney & Mc Kenna, 1979; Gaffney & Meylan, 1988; Gaffney, Meylan, & Wyss, 1991; Gauthier et al., 1988). The study of Gauthier et al. (1988) is probably the best documented study supporting close affinities between captorhinids and turtles:

     ======================================= Synapsida
     |
     |                                 ===== Millerettidae
     |                              ===|
     |                           ===|  ===== Pareiasauria
     |            ==parareptiles=|  |
     |            |              |  ======== Procolophonidae
     |            |              |
=====|            |              =========== Mesosauridae
     ==Sauropsida=|
                  |                     ==== Captorhinidae
                  |          ==Anapsida=|
                  |          |          ==== Testudines
                  ==Reptilia=|
                             |           ||| Protorothyrididae
                             ==Romeriida=|
                                         === Diapsida

This study is also significant in giving the first phylogenetic definitions for the names of many amniote taxa. In this tree, parareptiles are not closely related to turtles, but Gauthier et al. (1988) were not confident in this part of their tree (which is why they did not erect a formal Parareptilia).

Laurin & Reisz (1995) suggested that many of the taxa that Gauthier et al. (1988) considered parareptiles represented early relatives of turtles. Furthermore, Laurin & Reisz (1995) suggested that mesosaurs were the closest known relatives of reptiles:

     ==================================================== Synapsida
     |
     |            ======================================= Mesosauridae
     |            |
     |            |                         ============= Millerettidae
     |            |                         |
     |            |                         |  ========== Pareiasauria
     |            |          ==Parareptilia=|  |
=====|            |          |              ===|  ======= Procolophonidae
     ==Sauropsida=|          |                 ===|
                  ==Reptilia=|                    ======= Testudines
                             |
                             |            =============== Captorhinidae
                             |            |
                             ==Eureptilia=|           ||| Protorothyrididae
                                          ==Romeriida=|
                                                      === Diapsida

This study used a terminology derived from Olson (1947). Unfortunately, this terminology includes some junior synonyms (according to the rules of priority suggested by de Queiroz & Gauthier in 1990, 1992, and 1994) of the taxa defined by Gauthier et al. (1988) and the terminology used in the main phylogeny (in the page on Amniota) corrects this.

Lee (1995, 1996) studied in detail the phylogeny of the presumed relatives of turtles, and argued that pareiasaurs are the closest known relatives of turtles, rather than procolophonids (as argued by Laurin & Reisz, 1995). Furthermore, he believed that pareiasaurs are the stem-group of turtles (some pareiasaurs are more closely related to turtles than to other pareiasaurs). His phylogeny is as follows:


     ============================================================= Nyctiphruretia 
     |
     |                                       ===================== Owenettidae 
     |                    ==Procolophonoidea=|
     |                    |                  ===================== Procolophonids 
     |                    |
=====|                    |               ======================== Lanthanosuchids 
     ==Procolophoniformes=|               |
                          |               |                 ====== Sclerosaurus 
                          ==Hallucicrania=|                 |
                                          ==Pareiasauroidea=|  ||| Pareiasauria 
                                                            ===|
                                                               === Testudines 

All the studies mentioned above agree that turtles are the sister-clade of saurians among extant amniotes. However, the old idea that turtles are closely related to placodonts (Broom, 1924) has been revived recently (Rieppel, 1994, 1995; Rieppel & deBraga, 1996; deBraga & Rieppel, 1997). If this theory is accurate, turtles are saurians and are more closely related to lepidosaurs than to archosaurs.

     ================== Captorhinidae
     |
     |     ============ Pareiasauria
     |  ===|
     |  |  ============ Procolophonidae
     |  |
     |  |  ============ Araeoscelidia (a Permo-Carboniferous group of diapsids)
=====|  |  |
     ===|  |     ====== Lepidosauria
        |  |     |
        ===|  ===|  === Sauropterygia (a Mesozoic group of aquatic diapsids)
           ===|  ===|
              |     === Testudines
              |
              ========= Archosauromorpha

Amniote classification and characters supporting amniote phylogeny

An exhaustive list of autapomorphies of various amniote taxa cannot be provided here, but a sample of these characters can be given. The list given below assumes that the phylogeny presented at the beginning of the page on Amniota is essentially correct. Phylogenetic definitions, when available, are also given for the main taxa. Amniote classification can be summarized as such:

Amniota
   Synapsida
   Sauropsida
      Mesosauridae
      Reptilia
         Anapsida
            Millerettidae
            Unnamed
               Unnamed
                  Acleistorhinus
                  Lanthanosuchidae
               Unnamed
                  Macroleter
                  Nyctiphruretia
                  Procolophonia
                     Pareiasauria
                     Procolophonoidea
                     Testudines
         Romeriida
            Captorhinidae
            Unnamed
              "Protorothyrididae"
               Diapsida

Parts of the phylogeny are poorly documented (most of the unnamed clades) and will not be discussed below. Furthermore, if the suggestion of Modesto (1999) that mesosaurs are anapsids is accepted, this classification and the list of apomorphies will have to be modified.

Amniota is defined as "the most recent common ancestor of extant mammals and reptiles, and all its descendants" (Gauthier et al., 1988). It is divided into two stem-based taxa: Synapsida (mammals and their extinct relatives) and Sauropsida (reptiles and their fossil relatives). The autapomorphies of Amniota are listed in the "Characteristics" section of the Tree of Life page.

Sauropsida is defined as "reptiles plus all other amniotes more closely related to them than they are to mammals" (Gauthier, 1994). The characters supporting Sauropsida include the following:

Reptilia is defined as "the most recent common ancestor of extant turtles and saurians, and all of its descendants" (Gauthier et al., 1988). Characters supporting Reptilia include:

Click on an image to view larger version & data in a new window
Click on an image to view larger version & data in a new window

Figure 1. Amniote skulls in palatal view. A, Cotylorhynchus, a Lower Permian synapsid; B, Captorhinus, a Lower Permian romeriid; C, Procolophon, a Triassic anapsid; D, Proganochelys, the oldest known turtle (Upper Triassic). Redrawn from A, Laurin & Reisz (1995); B, Heaton (1979); C, Carroll & Lindsay (1985); and D, Gaffney (1990). Abbreviations: Bc, braincase; Ec, ectopterygoid; M, maxilla; N, nasal; Pa, palatine; Pm, premaxilla; Ps, parasphenoid; Pt, pterygoid; Q, quadrate; Qj, quadratojugal; S, stapes; Sq, squamosal; V, vomer.

Anapsida is defined as "extant turtles, and all other extinct taxa that are more closely related to them than they are to other [extant] reptiles" (Gauthier et al., 1988). Characters supporting Anapsida include:

Click on an image to view larger version & data in a new window
Click on an image to view larger version & data in a new window

Figure 2. Amniote skulls in lateral view. A, Cotylorhynchus, a Lower Permian synapsid; B, Captorhinus, a Lower Permian romeriid; C, Procolophon, a Triassic anapsid; D, Proganochelys, the oldest known turtle (Upper Triassic). Redrawn from A, Laurin & Reisz (1995); B, Heaton (1979); C, Carroll & Lindsay (1985); and D, Gaffney (1990). Abbreviations: Bc, braincase; E, epipterygoid; F, frontal; L, lacrimal; M, maxilla; N, nasal; P, parietal; Pm, premaxilla; Po, postorbital; Pof, postfrontal; Prf, prefrontal; Pt, pterygoid; Q, quadrate; Qj, quadratojugal; Sq, squamosal; St, supratemporal; T, tabular.

Click on an image to view larger version & data in a new window
Click on an image to view larger version & data in a new window

Figure 3. Skulls of early amniotes in dorsal view. A, Cotylorhynchus, a Lower Permian synapsid; B, Captorhinus, a Lower Permian romeriid; C, Procolophon, a Triassic anapsid; D, Proganochelys, the oldest known turtle (Upper Triassic). Redrawn from A, Laurin & Reisz (1995); B, Heaton (1979); C, Carroll & Lindsay (1985); and D, Gaffney (1990). Abbreviations: Bc, braincase; F, frontal; J, jugal; L, lacrimal; M, maxilla; N, nasal; P, parietal; Pa, palatal; Pm, premaxilla; Po, postorbital; Pof, postfrontal; Pp, postparietal; Prf, prefrontal; Qj, quadratojugal; Sq, squamosal; St, supratemporal; T, tabular.

Procolophonia is defined as "The most recent common ancestor of pareiasaurs, procolophonids, and testudines (Chelonia), and all its descendants" (Laurin & Reisz, 1995). It is diagnosed by several autapomorphies, including the following:

Romeriida is defined as "extant saurians, and all other taxa that are more closely related to them than they are to anapsids" (Gauthier et al., 1988). Romeriida possesses the following autapomorphies:

"Protorothyridids" and diapsids share the following synapomorphies:


We thank Miss Diane Scott for scanning the figures of amniote skulls, and Ms. Patricia Lai for proof-reading this page.

References

Broom R. 1924. On the classification of the reptiles. Bulletin of the American Museum of Natural History 51: 39-65.

Carroll R. L. & W. Lindsay. 1985. Cranial anatomy of the primitive reptile Procolophon. Canadian Journal of Earth Sciences 22: 1571-1587.

de Queiroz, K. & J. Gauthier. 1990. Phylogeny as a central principle in taxonomy: Phylogenetic definitions of taxon names. Systematic Zoology 39: 307-322.

de Queiroz, K. & J. Gauthier. 1992. Phylogenetic taxonomy. Annual Review of Ecology and Systematics 23: 449-480.

de Queiroz, K. & J. Gauthier. 1994. Toward a phylogenetic system of biological nomenclature. Trends in Ecology and Evolution 9: 27-31.

deBraga M. & O. Rieppel. 1997. Reptile phylogeny and the interrelationships of turtles. Zoological Journal of the Linnean Society 120: 281-354.

Gaffney E. S. 1990. The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the American Museum of Natural History 194: 263.

Gaffney, E. S. & M. C. Mc Kenna 1979. A Late Permian captorhinid from Rhodesia. American Museum Novitates 2688: 1-15.

Gaffney, E. S. & P. A. Meylan 1988. A phylogeny of turtles. In M. J. Benton (ed.) The Phylogeny and Classification of the Tetrapods: 157-219. Oxford: Clarendon Press.

Gaffney E. S., P. A. Meylan, & A. R. Wyss. 1991. A computer assisted analysis of the relationships of the higher categories of turtles. Cladistics 7: 313-335.

Gauthier J. A. 1994. The diversification of the amniotes. In: D. R. Prothero and R. M. Schoch (ed.) Major Features of Vertebrate Evolution: 129-159. Knoxville, Tennessee: The Paleontological Society.

Gauthier, J., A. G. Kluge, & T. Rowe. 1988. The early evolution of the Amniota. In M. J. Benton (ed.) The phylogeny and classification of the tetrapods, Volume 1: amphibians, reptiles, birds: 103-155. Oxford: Clarendon Press.

Heaton M. J. 1979. Cranial anatomy of primitive captorhinid reptiles from the Late Pennsylvanian and Early Permian Oklahoma and Texas. Bulletin of the Oklahoma Geological Survey 127: 1-84.

Laurin, M. & R. R. Reisz. 1995. A reevaluation of early amniote phylogeny. Zoological Journal of the Linnean Society 113: 165-223.

Lee, M. S. Y. 1995. Historical burden in systematics and the interrelationships of 'Parareptiles'. Biological Reviews of the Cambridge Philosophical Society 70: 459-547.

Lee M. S. Y. 1996. Correlated progression and the origin of turtles. Nature 379: 812-815.

Modesto S. P. 1999. Observations on the structure of the Early Permian reptile Stereosternum temidum Cope. Palaeontologia Africana 35: 7-19.

Olson E. C. 1947. The family Diadectidae and its bearing on the classification of reptiles. Fieldiana Geology 11: 1-53.

Rieppel, O. 1994. Osteology of Simosaurus gaillardoti and the relationships of stem-group sauropterygia. Fieldiana Geology 1462: 1-85.

Rieppel O. 1995. Studies on skeleton formation in reptiles: implications for turtle relationships. Zoology-Analysis of Complex Systems 98: 298-308.

Rieppel O. & M. deBraga. 1996. Turtles as diapsid reptiles. Nature 384: 453-455.

About This Page

Michel Laurin
Muséum National d'Histoire Naturelle, Paris, France

Jacques A. Gauthier
Yale University, New Haven, Connecticut, USA

Page: Tree of Life Phylogeny and Classification of Amniotes Authored by Michel Laurin and Jacques A. Gauthier. The TEXT of this page is licensed under the Creative Commons Attribution License - Version 3.0. Note that images and other media featured on this page are each governed by their own license, and they may or may not be available for reuse. Click on an image or a media link to access the media data window, which provides the relevant licensing information. For the general terms and conditions of ToL material reuse and redistribution, please see the Tree of Life Copyright Policies.

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