A primitive protostegid from Australia and early sea turtle evolution

Benjamin P Kear, Michael S.Y Lee

Abstract

Sea turtles (Chelonioidea) are a prominent group of modern marine reptiles whose early history is poorly understood. Analysis of exceptionally well preserved fossils of Bouliachelys suteri gen. et sp. nov., a large-bodied basal protostegid (primitive chelonioid) from the Early Cretaceous (Albian) of Australia, indicates that early sea turtles were both larger and more diverse than previously thought. The analysis implies at least five distinct sea turtle lineages existed around 100 million years ago. Currently, the postcranially primitive Ctenochelys and Toxochelys are interpreted as crown-group sea turtles closely related to living cheloniids (e.g. Chelonia); in contrast, the new phylogeny suggests that they are transitional (intermediate stem-taxa) between continental testudines and derived, pelagic chelonioids.

Keywords:

1. Introduction

Sea turtles (Chelonioidea) have a long fossil record stretching back to the late Early Cretaceous (late Aptian/early Albian, ca 105 Myr ago; see Hirayama 1998). However, their early evolutionary history remains largely unknown, as recent phylogenies do not recognize any definitive stem-group taxa. At present, all fossil sea turtles are assigned to one of two extant lineages within crown chelonioids (Hirayama 1994, 1997, 1998; Joyce et al. 2004; Lehman & Tomlinson 2004): one leads to living cheloniids (Pancheloniidae: Joyce et al. 2004), and the other to living Dermochelys (Pandermochelys: Joyce et al. 2004). The latter group includes the extinct Protostegidae, a diverse Cretaceous clade containing some spectacular Late Cretaceous giants (e.g. Archelon, possibly up to 4 m maximum length; Wieland 1896). The cranial morphology of protostegids is poorly known (Hooks 1998). However, here we report on several exceptionally well preserved skulls belonging to one of the stratigraphically oldest and most primitive protostegids yet found. A re-evaluation of sea turtle phylogeny incorporating these new fossils (re)establishes the primitive, shallow-water Toxochelys and Ctenochelys (Gaffney & Meylan 1988) as stem chelonioids; these taxa are currently placed within crown-chelonioids, along the lineage leading to living cheloniids (see Hirayama 1994, 1997, 1998).

2. Material and methods

Bouliachelys suteri gen. et sp. nov. (figure 1a–g and electronic supplementary material) was added to the most comprehensive published phylogenetic data set of sea turtles (Hirayama 1998), which was revised as follows. The chimera taxon Osteopygis was separated into two taxa (the cranial Euclastes and postcranial Osteopygis; Parham 2005), and additional postcranial characters for Euclastes scored from E. (Erquelinnesia) gosseleti (Lynch & Parham 2003; Hirayama 1994). Modifications were also made to the codings and/or character state definitions of 12 characters. A full matrix and character list with annotations discussing these points is provided in electronic supplementary material. Maximum parsimony trees, bootstrap frequencies (1000 replicates), and Bremer support were calculated using heuristic searches in phylogenetic analysis using parsimony (PAUP; Swofford 2000) employing 1000 random-addition replicates. Analyses performed with multi-state characters ordered or unordered (see electronic supplementary material) yielded similar results; the optimal tree (L=211) from the unordered analysis is shown in figure 2.

Figure 1

Skulls of Bouliachelys suteri gen. et sp. nov. (a) Holotype (QM F31669) skull, (b) parietal section, and (c) mandible in dorsal view. Referred (SAM P41106) (d) skull and (e) mandible in lateral, (f) dorsal and (g) ventral views (sutures highlighted). Additional photos can be found in the electronic supplementary material. Abbreviations: ang, angular; art, articular; bo, basioccipital; bs, basisphenoid; cor, coronoid; den, dentary; ex, exoccipital; fr, fontal; ju, jugal; mx, maxilla; na, nasal; op, opisthotic; pa, parietal; pal, palatine; pf, postfrontal; pm, premaxilla; po, postorbital; pr, prootic; pt, pterygoid; q, quadrate; qj, quadratojugal; so, supraoccipital; sur, surangular; vo, vomer.

Figure 2

Phylogeny and stratigraphic record of sea turtles, including Bouliachelys (see electronic supplementary material). Living lineages in black lines, extinct lineages in grey. Boxed numbers at selected nodes refer to synapomorphies discussed in the main text. Other numbers refer to bootstrap/Bremer support. The deep nesting of the ancient Santanachelys suggests the existence of at least five lineages in the Aptian (depending on how polytomies are resolved).

3. Phylogenetic taxonomy

All higher taxon names sensu Joyce et al. 2004.

Testudines Batsch, 1788; Chelonioidea Baur, 1893; Pandermochelys Joyce et al. (2004); Protostegidae Cope, 1872

B. suteri gen. et sp. nov.

(a) Etymology

After Boulia township, the most productive locality for this taxon (see below); and Richard and John Suter who discovered many of the specimens.

(b) Holotype, locality and horizon

Holotype (figure 1a–c) QM F31669 (Queensland Museum, Brisbane, Australia) from Dunraven Station, near Hughenden, central-northern Queensland, Australia; referred specimen (figure 1d–g) SAM P41106 (South Australian Museum, Adelaide, Australia) from Boulia region, western Queensland, Australia. Both localities are Toolebuc Formation (Rolling Downs Group), Eromanga Basin, latest middle to late Albian, P. ludbrookiae Zone/upper C. paradoxa–P. pannosus Zone (McMinn & Burger 1986; Alexander & Sansome 1996).

(c) Diagnosis

Identical for genus and species due to monotypy. Bouliachelys possesses the unique derived features (within chelonioids) of highly sculpted skull roof bones, a rugose boss anterior to each orbit, and double longitudinal keels (formed by the basisphenoid and pterygoids) on the ventral surface of the basicranium and palate. Bouliachelys differs from Notochelone (the only other Australian fossil sea turtle known from cranial remains) in several additional traits: it is larger, lacks a jugal-quadrate contact9, possesses hooked premaxillae13, and an upper triturating surface incorporating the palatine15 but not vomer16, a pterygoid excluded from the mandibular condyle24, and a basiphenoid-pterygoid with a V-shaped crest31 (character subscript numbering follows the data matrix in the electronic supplementary material, where distributions are scored across all chelonioids). Bouliachelys is distinguished from all other chelonioids in displaying a unique mosaic of primitive and derived features that suggest it is a basal protostegid (figure 2). All protostegids can be diagnosed by presence of nasal bones2, palatines meeting medially20, foramen palatinum posterius open posteriorly21, biconvex second or third cervical vertebra50, lateral process restricted to anterior surface of humerus shaft71, and a curved radius75 (c.f. Hirayama 1998). Santanachelys is the most basal known protostegid; Bouliachelys and later forms share the loss of the ventral cheek emargination12, and a strong lingual ridge of the maxilla19. Finally, protostegids above Santanchelys and Bouliachelys are united in having a triturating surface that excludes the palatine15 but includes the vomer16.

4. Evolutionary implications

A phylogenetic analysis of major sea turtle lineages, including Bouliachelys, was conducted (see electronic supplementary material). The traits discussed above robustly place Bouliachelys within crown (living) Chelonioidea, Pandermochelys and Protostegidae; and (with less certainty) suggest it is the most basal protostegid after Santanachelys (figure 2). While this phylogeny is similar to other previous studies (Hirayama 1998; Lehman & Tomlinson 2004), it is more pectinate. Toxochelys and Ctenochelys are no longer allied with derived Cheloniidae (sensu Hirayama 1994, 1997, 1998; Joyce et al. 2004; Lehman & Tomlinson 2004), but rather are reinterpreted as stem sea turtles outside crown Chelonioidea (an arrangement proposed elsewhere on braincase traits; see Gaffney and Meylan 1988; Hooks 1998). This hypothesis is further supported here by limb and girdle morphology, with Toxochelys and Ctenochelys retaining primitive postcranial features lost in crown chelonioids (figure 2): ischium with a well developed lateral process64, humerus with a capitellum that is upturned and shouldered68, first and second digits incorporated into paddle78, and femur with distinct trochanters79. The derived states of these postcranial characters—functionally related to pelagic natatory habits—thus appear only once and were present in the ancestor of crown chelonioids; consequently they do not need to evolve convergently in the lineages leading to living cheloniids and dermochelyids. The dorsally oriented orbits5 of Toxochelys and Ctenochelys also suggest that they retained the primitive condition of shallow-water and/or benthic habits (and potentially a less pelagic existence; c.f. Hirayama 1997); in contrast, the orbits of most crown chelonioids face laterally, implying a more ‘pelagic-adapted’ skull.

This new data clarifies other evolutionary trends within sea turtles. (i) The Australian fossil taxa are amongst the largest known before the Late Cretaceous; the skull of Bouliachelys suggests an animal some 50% larger than Notochelone (maximum adult body length reconstructed at less than 1 m; Molnar 1991); an even bigger sympatric taxon, Cratochelone (inferred maximum body length approaching 4 m; Longman 1915), is known from fragmentary postcranial remains only (Kear 2003). This shows that large body size in chelonioids was achieved very early in the group's history, some 25 Myr earlier (during the Albian ca 100 Myr ago, rather than Campanian ca 75 Myr ago) than commonly thought. (ii) Primitive protostegids (Bouliachelys, Santanachelys) have poorly developed secondary palates, demonstrating that this feature probably evolved convergently in advanced protostegids and cheloniids. (iii) The hooked beak (supposedly an adaptation for feeding on pelagic ammonites; Hirayama 1994, 1997) of Bouliachelys and more derived giant protostegids (e.g. Protostega) may also represent convergent adaptations. Finally, the phylogenetic position of the oldest-known sea turtle (the 105 Myr-old Santanachelys from the Aptian–Albian boundary; Hirayama 1998) indicates that a diversity of sea turtles existed during the Aptian, with at least five lineages present: these include Santanachelys, derived protostegids, dermochelyiids, cheloniids and the Toxochelys–Ctenochelys clade (Hirayama 1997).

Acknowledgements

The authors thank R. Suter (Stonehouse Museum, Boulia) and J. Suter (Sydney) for provision of specimens and information. T. & S. Hurley (Andamooka) also provided information and assistance in the field. R. Hamilton-Bruce (South Australian Museum) assisted with production of the figures. We also thank two anonymous referees for helpful comments. The Australian Research Council, South Australian Museum, Umoona Opal Mine and Museum, Coober Pedy, Outback at Isa Riversleigh Fossil Centre, Origin Energy, The Adelaide Advertiser newspaper, The SA museum Waterhouse Club, the Coober Pedy Tourism Association, Commercial and General Capital Ltd and Kenneth J. Herman Inc. provided financial support.

Footnotes

References

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