Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019 May 1;7:e6811.
doi: 10.7717/peerj.6811. eCollection 2019.

Anatomy of Rhinochelys pulchriceps (Protostegidae) and Marine Adaptation During the Early Evolution of Chelonioids

Affiliations
Free PMC article

Anatomy of Rhinochelys pulchriceps (Protostegidae) and Marine Adaptation During the Early Evolution of Chelonioids

Serjoscha W Evers et al. PeerJ. .
Free PMC article

Abstract

Knowledge of the early evolution of sea turtles (Chelonioidea) has been limited by conflicting phylogenetic hypotheses resulting from sparse taxon sampling and a superficial understanding of the morphology of key taxa. This limits our understanding of evolutionary adaptation to marine life in turtles, and in amniotes more broadly. One problematic group are the protostegids, Early-Late Cretaceous marine turtles that have been hypothesised to be either stem-cryptodires, stem-chelonioids, or crown-chelonioids. Different phylogenetic hypotheses for protostegids suggest different answers to key questions, including (1) the number of transitions to marine life in turtles, (2) the age of the chelonioid crown-group, and (3) patterns of skeletal evolution during marine adaptation. We present a detailed anatomical study of one of the earliest protostegids, Rhinochelys pulchriceps from the early Late Cretaceous of Europe, using high-resolution μCT. We synonymise all previously named European species and document the variation seen among them. A phylogeny of turtles with increased chelonioid taxon sampling and revised postcranial characters is provided, recovering protostegids as stem-chelonioids. Our results imply a mid Early Cretaceous origin of total-group chelonioids and an early Late Cretaceous age for crown-chelonioids, which may inform molecular clock analyses in future. Specialisations of the chelonioid flipper evolved in a stepwise-fashion, with innovations clustered into pulses at the origin of total-group chelonioids, and subsequently among dermochelyids, crown-cheloniids, and gigantic protostegids from the Late Cretaceous.

Keywords: Chelonioidea; Flipper evolution; Intraspecific variation; Marine adaptation; Neuroanatomy; Phylogeny; Protostegidae; Taxonomy.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. 3D renderings of the holotypes of UK species of Rhinochelys considered valid by Collins (1970).
(A) CAMSM B55775, the holotype of Rhinochelys pulchriceps, left lateral view; (B) as (A), but ventral view; (C) NHMUK PV OR43980, the holotype of R. cantabrigiensis, left lateral view; (D) as (B), but ventral view; (E) NHMUK PV R2226, the holotype of R. elegans, left lateral view; (F) as (E), but ventral view. Scale bars equal 20 mm.
Figure 2
Figure 2. Lateral views of cranium of CAMSM B55783.
(A) 3D rendering of left lateral view; (B) interpretative line drawing of (A); (C) 3D rendering of right lateral view; (D) interpretative line drawing of (C). Scale bar equals 10 mm. Note that bones are labelled in bold, and that the left squamosal, quadratojugal, and part of the postorbital in (A–B) are shown as a single model because sutures between these bones were unclear in the CT scan. Abbreviations: cty, cavum tympani; ex, exoccipital; f, frontal; fon, foramen orbito-nasale; j, jugal; mx, maxilla; na, nasal; op, opisthotic; or, orbit; pal, palatine; par, parietal; pjp, posterior jugal process; pmx, premaxilla; po, postorbital; prf, prefrontal; q, quadrate; qj, quadratojugal; soc, supraoccipital; sq, squamosal.
Figure 3
Figure 3. Dorsal and ventral views of cranium of CAMSM B55783.
(A) 3D rendering of dorsal view; (B) interpretative line drawing of (A); (C) 3D rendering of ventral view; (D) interpretative line drawing of (C). Scale bar equals 10 mm. Note that bones are labelled in bold. Abbreviations: ane, apertura narium externa; apni, aperture narium intera; boc, basioccipital; bt, basal tuber; ex, exoccipital; exptp, external pterygoid process, f, frontal; for, foramen; fpcci, foramen posterius canalis carotici interni; fpo, fenestra postotica; fpp, foramen posterius palatinum; j, jugal; labr, labial ridge; linr, lingual ridge; mc, mandibular condyle; mx, maxilla; na, nasal; op, opisthotic; or, orbit; pal, palatine; par, parietal; pbsph, parabasisphenoid; pmx, premaxilla; po, postorbital; prf, prefrontal, pt, pterygoid; qj, quadratojugal; q, quadrate; sq, squamosal; stf, subtemporal fossa; v, vomer.
Figure 4
Figure 4. Anterior and posterior views of cranium of CAMSM B55783.
(A) 3D rendering fo anterior view; (B) interpretative line drawing of (A); (C) 3D rendering of posterior view; (D) interpretative line drawing of (C). Scale bar equals 10 mm. Note that bones are labelled in bold. Abbreviations: ane, apertura narium externa; boc, basioccipital; bt, basal tuber; ex, exoccipital; f, frontal; fap, foramen antrum postoticum; fpo, fenestra postotica; ica, incisura columella auris; j, jugal; mx, maxilla; na, nasal; occ, occipital condyle; op, opisthotic; orm, orbital margin; par, parietal; pif, processus interfenestralis; po, postorbital; popr, paroccipital process; prf, prefrontal; pro, prootic; pt, pterygoid; q, quadrate; qj, quadratojugal; sq, squamosal; v, vomer.
Figure 5
Figure 5. Posterior view of partial anterior part of the cranium of CAMSM B55783 showing the region of the fissura ethmoidalis.
(A) 3D rendering; (B) interpretative line drawing. Scale bar equals five mm. Note that bones are labelled in bold. Abbreviations: f, frontal; feth, fissura ethmoidalis; fon, foramen orbito-nasale; olc, olfactory canal; prf, prefrontal; pal, palatine; sv, sulcus vomeri; v, vomer; vmpf, ventromedial process of frontal.
Figure 6
Figure 6. Comparison of frontals in dorsal view.
(A) 3D rendering of CAMSM B55775; (B) 3D rendering of CAMSM B55783. Scale bars equal five mm. Abbreviations: scs, scute sulcus.
Figure 7
Figure 7. Medial view of the left side of the partial anterior cranium of CAMSM B55783.
(A) 3D rendering; (B) interpretative line drawing. Scale bar equals five mm. Note that bones are labelled in bold. Abbreviations: apni, apertura narium interna; ch, choane; crci, crista cranii; f, frontal; feth, fissura ethmoidalis; fon, foramen orbito-nasale; ipxr, interpremaxillary recess; mx, maxilla; na, nasal; naf, nasal fossa; olc, olfactory canal; pal, palatine; prf, prefrontal; pmx, premaxilla; sol, sulcus olfactorius; vmpf, ventromedial process of frontal.
Figure 8
Figure 8. Partial left side of the braincase of NHMUK PV OR35197.
(A) 3D rendering; (B) interpretative line drawing. Note that bones are labelled in bold. Scale bar equals five mm. Abbreviations: epi p, epipterygoid process of quadrate; fcep, fossa cartilaginis epipterygoidei; par, parietal; pip, processus inferior parietalis; pro, prootic; pt, pterygoid; q, quadrate; tf, trigeminal foramen.
Figure 9
Figure 9. Comparison of left cheek regions showing differences in jugal morphology.
(A) 3D rendering of CAMSM B 55783; (B) 3D rendering of NHMUK PV OR35197. Scale bars equal five mm. Note that bones are labelled in bold, and that the left squamosal, quadratojugal, and part of the postorbital in (A) are shown as a single model because sutures between these bones were unclear in the CT scan. Abbreviations: j, jugal; pjp, posterior jugal process; po, popstorbital; qj, quadratojugal; sq, squamosal.
Figure 10
Figure 10. Dorsal view of palate and basicranium of CAMSM B55783.
(A) 3D rendering; (B) interpretative line drawing. Scale bar equals 10 mm. Note that bones are labelled in bold. Abbreviations: boc, basioccipital; ch, meatus choane; ex, exoccipital; exptp, external pterygoid process; fon, foramen orbito-nasale; fst, foramen stapedio-temporale; fpp, foramen palatinum posterius; j, jugal; lab, cavum labyrinthicum; mx, maxilla; occ, occipital condyle; naf, nasal fossa; op, opisthotic; orm, orbital margin; pal, palatine; pbsph, parabasisphenoid; pmx, premaxilla; pmx r, premaxilla ridge; pro, prootic; pt, pterygoid; pto, processus trochlearis oticum; q, quadrate; qj, quadratojugal; sptf, supratemporal fossa; stf, subtemporal fossa; v, vomer.
Figure 11
Figure 11. Comparison of quadrates in right lateral view.
(A) 3D rendering of right quadrate of CAMSM B55775; (B) 3D rendering of right quadrate of CAMSM B55776. Scale bars equal five mm. Abbreviations: cty, cavum tymani; fap, foramen antrum postoticum; ica, incisura columella auris.
Figure 12
Figure 12. Comparison of trochlear processes in anterior view.
(A) 3D rendering of right quadrate and prootic of NHMUK PV OR35197; (B) 3D rendering of right quadrate and prootic of CAMSM B55775. Scale bars equal two mm in (A) and five mm in (B). Abbreviations: epi p, epipterygoid process of quadrate; fcav, foramen cavernosum; pto pr, prootic portion of processus trochlearis oticum; pto q, quadrate portion of processus trochlearis oticum.
Figure 13
Figure 13. Pterygoids and parabasisphenoid of CAMSM B55783 in articulation.
(A) 3D rendering in dorsal view; (B) interpretative line drawing of (A); (C) 3D rendering in ventral view; (D) interpretative line drawing of (C); (E) 3D rendering in anterior view; (F) interpretative line drawing of (E). Scale bar equals five mm. Abbreviations: caj, cavum acustico-jugulare; ccav, canalis cavernosus; dptr, dorsal pterygoid ridge; ds, dorsum sellae; faccc, foramen anterius canalis carotici cerebralis; faccp, foramen anterius canalis carotici palatinum; fpcci, foramen posterius canalis carotici interni; pal f, palatine facet; ptf, pterygoid fossa; qp pt, quadrate process of pterygoid; scav, sulcus cavernosus; stur, sella turcica; tf, trigeminal foramen; vptc, ventral pterygoid ridge.
Figure 14
Figure 14. Comparison of right exoccipitals.
(A) 3D rendering of CAMSM B55775; (B) 3D rendering of CAMSM B55783. Scale bars equal three mm. Abbreviations: exco, exoccipital part of the condylus occipitalis; fm, foramen magnum; fpo, fenestra postotica; por, posterior ridge of exoccipital.
Figure 15
Figure 15. Basicranial details of CAMSM B55783.
(A) 3D rendering of basicranium in dorsal view; (B) interpretative line drawing of (A); (C) 3D rendering of the right otic capsule and partial basicranium in medial view; (D) interpretative line drawing of (C); (E) 3D rendering of cavum acustico-jugulare in posteroventrolateral view; (F), interpretative line drawing of (E). Scale bar in top row equals 10 mm, scale bar in middle and bottom row equal five mm. Note that bones are labelled in bold. Abbreviations: asc, anterior semicircular canal; boc, basicoccipital; bt, basal tuber; btb, basis tuberculi basalis; ccav, canalis cavernosus; cepi; cavum epitericum; ex, exoccipital; faccc, foramen anterius canalis carotici cerebralis; faf (VII; VIII), fossa acustico-facialis; fap, foramen antrum postoticum; fcav, foramen cavernosum; feng (IX), foramen externum nervi glossopharyngei; fing (IX), foramen internum nervi glossopharyngei; fja (X, XI), foramen jugulare anterius; fnf (VII), foramen nervi facialis; fnh (XII), foramina nervi hypoglossi; fpcci, foramen posterius canalis carotici interni; fpl, fenestra perilymphatica; fov, fenestra ovalis; fst, foramen stepadio-temporale; ica, incisura columalla auris; lab, cavum labyrinthicum; lsc, lateral semicircular canal; op, opisthotic; pbsph, parabasisphenoid; pif, processus interfenestralis; pro, prootic; prof (V), prootic foramen; psc, posterior semicircular canal; pt, pterygoid; q, quadrate; scav, sulcus cavernosus; tf (V1–2), trigeminal foramen.
Figure 16
Figure 16. 3D renderings of the mandibles of Rhinochelys.
(A) 3D renderings of right mandibular ramus of CAMSM B55776 in lateral view; (B) medial view; (C) posterior view; (D) 3D renderings of the mandible of CAMSM B55783 in dorsal view; (E) posterior view; (F) left lateral view. All scale bars equal five mm. Note that bones are labelled in bold. Abbreviations: aimf, anterior intermandibular foramen; ang, angular; ap pra, anterior process of prearticular; art, articular; cor, coronoid; cor p, coronoid process; den, dentary; dep, depression; fai, foramen alveolare inferius; fm, Meckellian fossa; fnat, foramen nervi auricolotemporalis; for, foramen; labr, labial ridge; medr, median dentary ridge; mimf, medial intermanibular foramen; pimf, posterior intermandibular foramen; pra, prearticular; pra f, prearticular facet; scm, sulcus for the Meckelian cartilage; spl, splenial; sur, surangular; texp, triangular expansion; tris, triturating surface.
Figure 17
Figure 17. Comparison of surangulars.
(A) 3D rendering of right surangular of CAMSM B55776 in lateral view; (B) 3D rendering of left surangular of CAMSM B55783 in lateral view, reflected for comparison; (C) 3D rendering of right surangular of CAMSM B55776 in medial view; (D) 3D rendering of left surangular of CAMSM B55783 in medial view, reflected for comparison. Scale bars equal three mm. Abbreviations: ap sur, anterior process of surangular; cor f, coronoid facet; fnat, foramen nervi auricolotemporalis, fnat lam, foramen nervi auricolotemporalis lamina.
Figure 18
Figure 18. Consensus trees of our phylogenetic analysis.
(A) strict consensus tree of >10,000 MPTs. (B) reduced strict consensus tree obtained by pruning the Sinemys clade (Sinemys lens + Sinemys gamera), Erquelinnesia gosseleti and Oligochelone rupelensis.
Figure 19
Figure 19. Distribution of specimens of Rhinochelys (n = 27) in cranial geometry morphospaces recovered by Principal Component Analysis of seven cranial measurements.
(A) PC1 vs. PC2; (B) PC1 vs. PC3.
Figure 20
Figure 20. Cranial specimens from the Cambridge Greensand Member of the West Melbury Marly Chalk Formation that cannot be referred to Rhinochelys.
(A) CAMSM B55802 in dorsal view; (B) CAMSM B55802 in anteroventral view; (C) CAMSM B55802 in posterior view; (D) CAMSM B56338 in dorsal view; (E) CAMSM B56338 in ventral view; (F) CAMSM B56338 in left lateral view; (G) CAMSM B56338 in anterior view. Scale bars equal 20 mm. Abbreviations: cav, cavity on the anterior surface of the triturating surface; inn, internal naris; lr, labial ridge; par-pto, parietal contribution to the processus trochlearis oticum; parr, parietal ridge; v, vomer.
Figure 21
Figure 21. Comparisons of mandibular morphotypes from the Cambridge Greensand Member of the West Melbury Marly Chalk Formation.
(A) Rhinochelys pulchriceps morphotype, 3D rendering of partial mandible of CAMSM B59560 in right anterodorsolateral view, reflected for comparison; (B) morphotype 1, 3D rendering of partial mandible of CAMSM B55848 in left anterodorsolateral view; (C) morphotype 2, 3D rendering of partial mandible of CAMSM B55860 in left anterodorsolateral view; (D) morphotype 3, 3D rendering of partial mandible of CAMSM B56586 in left anterodorsolateral view. Scale bars equal 20 mm.
Figure 22
Figure 22. Comparisons of humeri morphotypes from the Cambridge Greensand Member of the West Melbury Marly Chalk Formation.
(A) morphotype 1, left humerus of CAMSM B56168 in ventral view; (B) morphotype 2, left humerus of CAMSM B55987 in ventral view; (C) morphotype 3, left humerus of CAMSM B55988 in ventral view; (D) as in (A), but dorsal view; (E) as in (B), but dorsal view; (F) as (C), but dorsal view. Scale bars equal 20 mm. Abbreviations: ch, caput humeri; eecg, ectepicondylar groove; hlp, lateral process of humerus; hmp, medial process of humerus; pas, preaxial shoulder.
Figure 23
Figure 23. Simplified reduced strict consensus tree scaled to geologic time using range data for turtles.
Figure 24
Figure 24. Simplified topology of chelonioids with character state transitions mapped onto the tree.
The topology is the one used for character optimisation and represents one MPT from the original analysis that is consistent with the topology of a 50% majority rule consensus tree. Boxes with crosses represent unambiguous character transitions, open boxes represent DELTRAN, and shaded boxes represent ACCTRAN. Numbers above boxes represent character numbers, numbers below boxes show the apomorphic state. For plesiomorphic states, please refer to Table 4. Line drawings represent schematic flipper morphology for specific OTUs (top row), and the generalised flipper morphology of early cheloniids (bottom right). Note that Roman letters denote digits and Arabic numbers denote phalangeal position. Abbreviations: c, centrale; dc, distal carpal; im, intermedium; mc, metacarpal; pi, pisiform; ulc, ulnare.

Similar articles

See all similar articles

Cited by 3 articles

References

    1. Albrecht PW. The cranial arteries of turtles and their evolutionary significance. Journal of Morphology. 1976;149(2):159–182. doi: 10.1002/jmor.1051490203. - DOI - PubMed
    1. Ali F, Zelenitzky DK, Therrien R, Weishampel D. Homology of the “ethmoid complex” of tyrannosaurids and its implications for the reconstruction of the olfactory apparatus of non-avian theropods. Journal of Vertebrate Paleontology. 2008;28(1):123–133. doi: 10.1671/0272-4634(2008)28[123:HOTECO]2.0.CO;2. - DOI
    1. Anquetin J. Reassessment of the phylogenetic interrelationships of basal turtles (Testudinata) Journal of Systematic Palaeontology. 2012;10(1):3–45. doi: 10.1080/14772019.2011.558928. - DOI
    1. Anquetin J, Püntener C, Billon-Bruyat J-P. Portlandemys gracilis n. sp., a new coastal marine turtle from the late Jurassic of Porrentruy (Switzerland) and a reconsideration of plesiochelyid cranial anatomy. PLOS ONE. 2015;10(6):e0129193 doi: 10.1371/journal.pone.0129193. - DOI - PMC - PubMed
    1. Anquetin J, Püntener C, Joyce WG. A review of the fossil record of Turtles of the Clade Thalassochelydia. Bulletin of the Peabody Museum of Natural History. 2017;58(2):317–369. doi: 10.3374/014.058.0205. - DOI

Grant support

This research was supported by a NERC studentship to Serjoscha Evers on the DTP Environmental Research (NE/L0021612/1), the Oxford Univeristy RCUK Block Grant, and a University College Old Member’s Trust Academic Travel Fund awarded to Serjoscha Evers. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

LinkOut - more resources

Feedback