Abstract
Internal carotid circulation is arguably one of the most intensively analyzed morphological characters in turtle systematics and, thus, it is critical for understanding turtle phylogeny. I used landmark-based geometric morphometrics to facilitate a quantitative analysis of variation in turtle skull shape and osteological correlates of the internal carotid circulation. The analysis indicates that the position of the foramen posterior canalis carotici interni differs among eucryptodires, paracryptodires, and pleurodires, but remains relatively stable within these lineages. This supports the hypothesis that the position of the foramen posterior canalis carotici interni is a reliable character for identifying higher turtle taxa. Results from the geometric morphometric analysis are consistent with two of the three traits recently proposed to affect patterns of internal carotid circulation. However, these three traits do not fully explain six different patterns of internal carotid circulation in turtles. I identify the association between the internal carotid artery and the palatine branch of the facial nerve (CN VII) as a developmental constraint in turtles. Using this association as a reference point, embryological observations reported in the literature suggest morphogenetic processes that may govern different patterns of internal carotid circulation. When mapped on a phylogenetic tree, some characters transform more than once independently. The evolution of internal carotid circulation in turtles may have been even more complex than reconstructed in this paper, because of uncertain relationships among basal eucryptodires and because of a mosaic of character states in that critical part of the tree.
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Acknowledgments
A project like this would not have been possible without the precise, consistent, and well-illustrated descriptive works by Eugene Gaffney (American Museum of Natural History) throughout his career. Ren Hirayama (Waseda University) encouraged me in the after-hours party at an annual meeting of the Society of Vertebrate Paleontology in 2008 to do a turtle project as a reprieve from my immersion in dinosaurs, which eventually led to this paper. Heather Jamniczky (University of Calgary) sent her publications and Lara Shychoski (University of Alberta) lent her copy of Zelditch et al. (2004). Don Brinkman and Dennis Braman (Royal Tyrrell Museum of Palaeontology) provided logistical support when the preliminary version of this project was presented in the Gaffney Turtle Symposium. I thank the editors for the additional time they provided to put my thoughts together for this project. Jim Gardner (Royal Tyrrell Museum of Palaeontology) handled the manuscript. Reviews by Larry Powell (University of Calgary), Juliana Sterli (Museo Paleontológico Egidio Feruglio), and an anonymous person substantially improved the paper. Rich Palmer and Richard Fox (both University of Alberta) carefully critiqued and edited earlier versions of the manuscript. I thank Kesia Andressen for her medical support. Financial assistance came from the Alberta Ingenuity Fund and from Junichi and Kanae Miyashita.
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Appendix
Appendix
List of the 132 taxa and sources for the 145 skull images used for this study. The classification of turtles largely follows Gaffney et al. (2006) and Joyce (2007). All clades higher than family level, except for the crown groups, are stem-based. Within each family, genera and species are listed alphabetically. For each species, the skull image used for this study can be found in the publication cited in the corresponding source section. In some cases (e.g., Gaffney 1979b), those images were reprinted from an earlier publication. Abbreviations in column headings: n, number of skull images; p, patterns based on Sterli and de la Fuente (2010). An asterisk (*) denotes taxa that Sterli et al. (2010) stated likely exhibited pattern V; however, until a detailed description is presented that verifies the lack of the foramen posterior canalis carotici interni in these taxa, for the purposes of this study they are tentatively assigned pattern II. The latter is a traditional intepretation for paracryptodires and is consistent with the placement of those genera within that major clade.
Taxon |
| n | p | Sources |
---|---|---|---|---|
Testudines | ||||
Proganochelys quenstedti | 1 | VI | Gaffney and Meeker (1983) | |
Kayentachelys aprix | 1 | VI | Gaffney et al. (1987) | |
Meiolania platyceps | 1 | IV | Gaffney (1983) | |
Mongolochelys efremovi | 2 | V | ||
Crown-group Testudines | ||||
Pleurodira | ||||
Chelidae | ||||
Batrachemys dahlia | 1 | III | Gaffney (1977) | |
Chelodina expansa | 1 | III | Gaffney (1977) | |
Chelus fimbriata | 1 | III | Gaffney (1977) | |
Emydura macquarrii | 1 | III | Gaffney (1977) | |
Hydromedusa tecifera | 1 | III | Gaffney (1977) | |
Mesoclemys gibba | 1 | III | Gaffney (1977) | |
Platemys platycephala | 1 | III | Gaffney (1977) | |
Pseudemydura umbrina | 1 | III | Gaffney (1977) | |
Pelomedusoidea | ||||
Pelomedusidae | ||||
Erymnochelys madagascariensis | 1 | III | Gaffney (1979b) | |
Pelomedusa subrufa | 1 | III | Gaffney (1979b) | |
Peltocephalus dumeriliana | 1 | III | Gaffney (1979b) | |
Pelusios sp. | 1 | III | Gaffney (1975a) | |
Pelusios niger | 1 | III | Gaffney (1979b) | |
Shweboemys antiqua | 1 | III | Wood (1970) | |
Araripemydidae | ||||
Araripemys barretoi | 2 | III | ||
Euraxemydidae | ||||
Dirqadim schaefferi | 1 | III | Gaffney et al. (2006) | |
Euraxemys essweini | 1 | III | Gaffney et al. (2006) | |
Podocnemidoidea | ||||
Podocnemididae | ||||
Bairdemys venezuelensis | 1 | III | Gaffney and Wood (2002) | |
Caninemys tridentata | 1 | III | Meylan et al. (2009) | |
Dacquemys paleomorpha | 2 | III | ||
Podocnemis expansa | 1 | III | Gaffney (1979b) | |
Bothremydidae | ||||
Acleistochelys mallensis | 1 | III | Gaffney et al. (2007a) | |
Araiochelys hirayamai | 1 | III | Gaffney et al. (2006) | |
Arenila krebsi | 1 | III | Gaffney et al. (2006) | |
Azabbaremys moragjonesi | 1 | III | Gaffney et al. (2001b) | |
Bothremys kellyi | 1 | III | Gaffney et al. (2006) | |
Bothremys maghrebiana | 1 | III | Gaffney et al. (2006) | |
Cearachelys placidoi | 1 | III | Gaffney et al. (2001a) | |
Foxemys mechinorum | 1 | III | Gaffney et al. (2006) | |
Kurmademys kallamedensis | 1 | III | Gaffney et al. (2001c) | |
Labrostochelys galkini | 1 | III | Gaffney et al. (2006) | |
Phosphatochelys tedfordi | 1 | III | Gaffney and Tong (2003) | |
Polysternon provinciale | 1 | III | Gaffney et al. (2006) | |
Sankuchemys sethnai | 1 | III | Gaffney et al. (2003) | |
Taphrosphys congolensis | 1 | III | Gaffney et al. (2006) | |
Taphrosphys ippolitoi | 1 | III | Gaffney et al. (2006) | |
Zalhafah bella | 1 | III | Gaffney et al. (2006) | |
Paracryptodira | ||||
Dorsetochelys delairi | 1 | II* | Evans and Kemp (1975) | |
Pleurosternidae | ||||
Pleurosternon bullocki | 1 | V | Sterli et al. (2010) | |
Glyptopsidae | ||||
Glyptops plicatulus | 1 | V | Gaffney (1979a) | |
Mesochelys durlstonensis | 1 | II* | Gaffney (1979a) | |
Baenidae | ||||
Baena arenosa | 1 | II | Gaffney (1972b) | |
Boremys pulchra | 1 | II | Brinkman and Nicholls (1991) | |
Cedorbaena putorius | 1 | II | Lyson and Joyce (2009b) | |
Chisternon undatum | 1 | II | Gaffney (1972b) | |
Eubaena cephalica | 1 | II | Gaffney (1972b) | |
Palatobaena sp. | 1 | II | Gaffney (1972b) | |
Palatobaena cohen | 4 | II | Lyson and Joyce (2009a) | |
Peckemys brinkman | 2 | II | Lyson and Joyce (2009b) | |
Plesiobaena antiqua | 2 | II | ||
Plesiobaena putorius | 1 | II | Gaffney (1972b) | |
Stygiochelys estesi | 1 | II | Gaffney (1972b) | |
Trinitichelys hiatti | 1 | II | Gaffney (1972b) | |
Eucryptodira | ||||
Plesiochelyidae | ||||
Plesiochelys etalloni | 1 | I | Gaffney (1975c) | |
Portlandemys mcdowelli | 1 | I | Gaffney (1975c) | |
Eurysternidae | ||||
Angolachelys mbaxi | 1 | I | Mateus et al. (2009) | |
Solnhofia parsonsi | 1 | I | Gaffney (1975d) | |
Thalassemys moseri | 1 | IV | Rieppel (1980) | |
Sinemyidae/Macrobaenidae | ||||
Chubutemys coppelloi | 1 | IV | Gaffney et al. (2007b) | |
Dracochelys bicuspis | 1 | IV | Gaffney and Ye (1992) | |
Hangaiemys hoburensis | 1 | IV | Sukhanov (2000) | |
Judithemys sukhanovi | 1 | IV | Parham and Hutchison (2003) | |
Sinemys gamera | 1 | IV | Sukhanov (2000) | |
Crown-group Cryptodira | ||||
Toxochelyidae | ||||
Toxochelys latiremis | 1 | I | Gaffney (1979b) | |
Cheloniidae | ||||
Caretta caretta | 1 | I | Carr (1952) | |
Chelonia mydas | 1 | I | Carr (1952) | |
Eochelone brabantica | 1 | I | Gaffney (1979b) | |
Eretmochelys imbricata | 1 | I | Carr (1952) | |
Euclastes acutirostris | 1 | I | Jaril et al. (2009) | |
Lepidochelys kempi | 2 | I | ||
Dermochelyidae | ||||
Dermochelys coriacea | 1 | I | Gaffney (1979b) | |
Chelydridae | ||||
Chelydra serpentina | 1 | I | Gaffney (1972a) | |
Macroclemys temminckii | 1 | I | Gaffney (1975b) | |
Platysternon megacephalum | 1 | I | Gaffney (1975b) | |
Protochelydra zangerli | 1 | I | Erickson (1973) | |
Lindholmemydidae | ||||
Mongolemys sp. | 1 | IV | Sukhanov (2000) | |
Testudinoidea | ||||
Emydidae | ||||
Chrysemys alabamensis | 1 | I | Gaffney (1979b) | |
Chrysemys concinna | 1 | I | Gaffney (1979b) | |
Chrysemys idahoensis | 1 | I | McDowell (1964) | |
Clemmys insculpta | 1 | I | Gaffney (1979b) | |
Deirochelys reticularia | 1 | I | Gaffney (1979b) | |
Emys orbicularis | 1 | I | Gaffney (1979b) | |
Malaclemys terrapin | 1 | I | Gaffney (1979b) | |
Malayemys subtrijuga | 1 | I | Gaffney (1979b) | |
Pseudemys texana | 3 | I | ||
Terrapene ornata | 1 | I | Gaffney (1979b) | |
Geoemydidae | ||||
Batagur baska | 1 | I | Gaffney (1979b) | |
Callagur borneoensis | 1 | I | Gaffney (1979b) | |
Chinemys reevesi | 1 | I | Gaffney (1979b) | |
Cuora trifasciata | 1 | I | Gaffney (1979b) | |
Geoclemys hamiltoni | 1 | I | McDowell (1964) | |
Geoemyda sp. | 1 | I | Gaffney (1979b) | |
Hardella thurgii | 1 | I | McDowell (1964) | |
Hieremys annandalii | 1 | I | Gaffney (1979b) | |
Kachuga smithii | 1 | I | Gaffney (1979b) | |
Mauremys mutica | 1 | I | Gaffney (1979b) | |
Melanochelys trijuga | 1 | I | Gaffney (1979b) | |
Morenia ocellata | 1 | I | Gaffney (1979b) | |
Ocadia sinensis | 1 | I | Gaffney (1979b) | |
Orlitia borneensis | 1 | I | Baur (1896) | |
Rhinoclemys annulata | 1 | I | Gaffney (1979b) | |
Siebenrockiella crassicollis | 1 | I | McDowell (1964) | |
Testudinidae | ||||
Geochelone elephantopus | 1 | I | Gaffney (1979b) | |
Gopherus polyphemus | 1 | I | Gaffney (1979b) | |
Homopus areolatus | 1 | I | Gaffney (1979b) | |
Kinixys horneana | 1 | I | Gaffney (1979b) | |
Malacochersus tornieri | 1 | I | Gaffney (1979b) | |
Pyxis arachnoides | 1 | I | Gaffney (1979b) | |
Testudo graeca | 1 | I | Gaffney (1979b) | |
Trionychoidea | ||||
Adocidae | ||||
Adocus sp. | 1 | I | Gaffney (1979b) | |
Adocus sp. | 1 | I | Meylan and Gaffney (1989) | |
Kinosternoidea | ||||
Dermatemydidae | ||||
Dermatemys mawii | 1 | I | Gaffney (1979a) | |
Dermatemys sp. | 1 | I | Meylan and Gaffney (1989) | |
Kinosternidae | ||||
Claudius augustatus | 1 | I | Gaffney (1979a) | |
Kinosternon subrubrum | 1 | I | Gaffney (1979a) | |
Staurotypus salvinii | 1 | I | Williams (1952) | |
Sternotherus odoratus | 3 | I | ||
Trionychia | ||||
Carettochelyidae | ||||
Carettochelys insculpta | 1 | I | Gaffney (1979b) | |
Pseudanosteira sp. | 1 | I | Gaffney (1979b) | |
Puppigerus camperi | 1 | I | Gaffney (1979b) | |
Trionychidae | ||||
Aspideretoides splendidus | 1 | I | Gardner et al. (1995) | |
Chitra indica | 1 | I | Gray (1855) | |
Cyclanorbis senegalensis | 1 | I | Loveridge and Williams (1957) | |
Cycloderma frenatum | 1 | I | Loveridge and Williams (1957) | |
Lissemys punctata | 1 | I | Gaffney (1979b) | |
Pelochelys bibroni | 1 | I | Gaffney (1979b) | |
Plastomenus thomasi | 1 | I | Gaffney (1979b) | |
Trionyx triunguis | 1 | I | Gaffney (1979b) |
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Miyashita, T. (2013). Geometric and Developmental Perspectives on the Evolution of the Skull and Internal Carotid Circulation in Turtles. In: Brinkman, D., Holroyd, P., Gardner, J. (eds) Morphology and Evolution of Turtles. Vertebrate Paleobiology and Paleoanthropology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4309-0_7
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