The oldest cynodont: new clues on the origin and early diversification of the Cynodontia

INTRODUCTION

The Cynodontia has long been recognized as a crucial therapsid group because it includes mammals as its extant subclade (Rubidge & Sidor, 2001). Extinct members of the group form a paraphyletic assemblage known as non-mammaliaform cynodonts and represent the stage at which many mammalian characteristics first appeared in therapsids. The earliest cynodont records are known from the latest Late Permian and include the genera Procynosuchus from South Africa, Tanzania, Germany and Russia (Kemp, 1979; Sues & Boy, 1988; Rubidge, 1995; Tatarinov, 2004), Cynosaurus and Nanictosaurus from South Africa (Rubidge, 1995; Van Heerden & Rubidge, 1990), and Dvinia, Uralocynodon and Nanocynodon from Russia (Tatarinov, 1968, 1987; Battail & Surkov, 2000). Procynosuchus is traditionally recognized as the earliest known cynodont (Rubidge & Sidor, 2001; Sidor & Smith, 2004) ranging from the base to the top of the Dicynodon Assemblage Zone [AZ] (Wuchiapingian–Changhsingian) in South Africa (Rubidge, 1995; Sidor & Smith, 2004) and in biostratigraphically equivalent levels in East Africa, western Germany (von Huene, 1950; Kemp, 1979; Sues & Boy, 1988) and Russia (=Cyrbasiodon; Tatarinov, 2004). A new cynodont from the older Tropidostoma AZ (early Late Permian) described here indicates a South African origin for cynodonts.

MATERIAL AND METHODS

The specimen described herein, SAM-PK-K10369 (in the collections of the Iziko: South African Museum, Cape Town, South Africa), consists of a complete, laterally compressed skull, a partially preserved axis and third cervical vertebra, and articulated femur, tibia and fibula. Institutional abbreviations and specimens of the therocephalians and basal cynodonts studied for comparative purposes are presented in Appendices 1 and 2, respectively.

A cladistic analysis using the program TNT (Goloboff, Farris & Nixon, 2003) was performed to determine the phylogenetic position of Charassognathus. A data matrix was constructed for 59 cranio-dental characters and 18 theriodont taxa. Cyonosaurus, ‘one of the rare gorgonopsian skulls to have been thoroughly studied’ (Sigogneau-Russell, 1989: 83), was used to root the cladograms. In addition to ten cynodont taxa, seven therocephalian taxa were included in the analysis, as Therocephalia is a sister group of the Cynodontia. A heuristic search was performed with all characters having equal weights. This search consisted of ten random addition sequences (ten Wagner trees randomizing the order of the terminals) and tree-bisection-reconnection swapping, storing ten trees per replication. The run was performed with collapsing rule one (Coddington & Scharff, 1994), which collapses branches with ambiguous support. Increasing the number of replicates did not change the result obtained. A second analysis was performed with similar settings, but using implied weights (Goloboff, 1993). The weighting was made by means of a constant of concavity K. A possible outcome is the decrease in the number of most parsimonious trees by reducing the influence of homoplastic characters. Characters showing many extra steps in the most parsimonious trees are thus down-weighted in relation to the characters that better fit those trees. Analyses were performed with the constant of concavity set at intermediate and low values.

Material examined and literature consulted for each taxon included in the cladistic analysis is presented in Appendix 2, the list of characters and data matrix in Appendix 3, and unambiguous synapomorphies for nodes of the most parsimonious tree obtained with implied weights are presented in Appendix 4.

SYSTEMATIC PALAEONTOLOGY

Therapsida Broom, 1905
Cynodontia Owen, 1861
Charassognathus gracilisgen. et sp. nov.

Diagnosis: This new cynodont is distinguished by the presence of a small notch in the base of the coronoid process, located in a similar position to the base of the masseteric fossa in Dvinia and Procynosuchus. The angle of the dentary is prominent, appearing more developed than in Procynosuchus and Dvinia, but less so than in Nanictosaurus. The dental formula is ?4·1· 8/3·1·?, and it is distinguished from Procynosuchus and Dvinia by the absence of maxillary precanine teeth. The anterior postcanines have a single high cusp in labial view, whereas the posterior postcanines exhibit a main cusp directed slightly backward, and tiny anterior and posterior accessory cusps, with the anterior accessory cusps positioned slightly higher than the posterior accessory cusps.

Comments: The combined presence of the following characters indicates that C. gracilis is a cynodont: multicuspidated postcanines; groove in the squamosal for the quadratojugal; two occipital condyles; elongated ascending process of the epipterygoid; frontal excluded from the orbital margin; prominent angle of the dentary; reflected laminar of the angular with small lateral crests and femoral head set off dorsally from the shaft (see Description for more details).

Holotype: SAM-PK-K10369 consists of a complete skull with lower jaw in occlusion, the axis, third cervical vertebra, ?cervical ribs and a few indeterminate bones. Associated material includes a right articulated femur, tibia and fibula.

Etymology: Greek, charasso, prefix meaning ‘notch’ and gnathus, ‘jaw’, referring to the characteristic notch on the dentary. The specific epithet, gracilis, Latin, meaning ‘slender’, refers to the delicate nature of the specimen.

Locality and horizon: The specimen was found in a roadside cutting of highway R353 in Teekloof Pass, between the towns Leeu Gamka and Fraserburg in the Beaufort West District, Western Cape Province, South Africa. The locality lies on the farm Willowdene, a portion of Beato 238 (Fig. 1); exact coordinates are given in the Iziko South African Museum. It is stratigraphically positioned in the upper half of a thick mudrock-dominated succession of fluvio-lacustrine strata, known locally as the Hoedemaker Member of the Teekloof Formation (Rubidge, 1995; 1, 2), which is considered to be early Late Permian (Wuchiapingian) in age (Catuneanu et al., 2005). The few laterally extensive sandstone bodies in the Hoedemaker Member (Fig. 2B) are interpreted as having been deposited as amalgamated point bars within high-sinuosity Mississippi-sized meandering rivers (Smith, 1987). Most of the vertebrate fossils are found in the thick greenish-grey massively bedded siltstone with minor mudstone intercalations that occur between the main channel sandstones. These sediments occur in 5–10-m-thick coarsening-upward sequences interpreted as prograding crevasse splay sequences. They were laid down by repeated overbank flood events emanating from the channel banks and ponding in the lowland flood basins. The new cynodont specimen was recovered from a 0.25-m-thick lens of fissile, dark purple, mudstone on a parting between two 1-m-thick beds of massive grey siltstone with purple mottles. The massive siltstones contain scattered oblate pedogenic carbonate nodules and are interpreted as proximal floodplain deposits laid down at the base of the meanderbelt slope. The fissile mudstone interlayer in which the study specimen was found is interpreted as a small pond deposit within the splay sequence.

Numerous skulls and skeletons of Diictodon galeops, along with other dicynodonts, namely Oudenodon baini, Emydops minor and Pristerodon mackayi, and, most significantly, the biozone indicator fossil Tropidostoma microtrema were collected from nearby outcrops (see Fig. 1B and Table 1). The gorgonopsians Lycaenops ornatus and Cyonosaurus longiceps, the therocephalian Ictidosuchoides longiceps and a new burnetiamorph comprise the carnivore fossil fauna collected in the vicinity. The presence of Tropidostoma as well as the abundant Diictodon galeops, and the absences of Pristerognathus, which characterizes the underlying zone, and Cistecephalus and Aulacephalodon from the succeeding biozone, biostratigraphically positions this specimen in the upper half of the 180-m-thick Tropidostoma Assemblage Zone (Rubidge, 1995).

Table 1. Localities and taxonomic identification of fossils from the Teekloof Pass between the towns Leeu Gamka and Fraserburg in the Beaufort West District, Western Cape Province. The Hoedemaker Member of the Beaufort Group outcrops in these localities (see Fig. 1)

Locality (see Fig. 1)	Identification
1	Diictodon galeops (SAM-PK-K6820)
2	2 Diictodon galeops (SAM-PK-K6818, K6819)
3	Diictodon galeops (SAM-PK-K6817)
4	4 Diictodon galeops (SAM-PK-K6821, K6822, K6827, K6887)
	2 Dicynodontia (SAM-PK-K6823, K6826)
	Emydops minor (SAM-PK-K6824)
	Pristerodon mackayi (SAM-PK-K6825)
5	Oudenodon baini (SAM-PK-K6834)
	Lycaenops ornatus (SAM-PK-K6835)
6	4 Diictodon galeops (SAM-PK-K6828, K6829, K6831, K6832)
	Dicynodontia (SAM-PK-K6830)
	Emydops minor (SAM-PK-K6833)
7	Pristerodon mackayi (SAM-PK-K8301)
	Diictodon galeops (SAM-PK-K8306)
8	15 Diictodon galeops (SAM-PK-K6763, K6765-K6778)
	Dicynodontia (SAM-PK-K6764)
9	6 Diictodon galeops (SAM-PK-K6754, K6755, K6757, K6759, K6761, K6762)
	Tropidostoma microtrema (SAM-PK-K6756)
	2 Dicynodontia (SAM-PK-K6758, K6760)
10	22 Diictodon galeops (SAM-PK-K6782-K6794, K6798, K6799, K6801, K6803-K6807, K6816)
	5 Tropidostoma microtrema (SAM-PK-K6795, K6796, K6797, K6808, K6809)
	Oudenodon baini (SAM-PK-K6800)
	Cyonosaurus longiceps (SAM-PK-K6802)
11	Emydops minor (SAM-PK-K6779)
	Dicynodontia (SAM-PK-K6780)
	Diictodon galeops (SAM-PK-K6781)
12	15 Diictodon galeops (SAM-PK-K6652-K6654, K6656, K6658-K6663, K6665-K6669)
	Burnetiamorpha (SAM-PK-K6655)
	Tropidostoma microtrema (SAM-PK-K6657)
	Dicynodontia (SAM-PK-K6664)
	Ictidosuchoides longiceps (SAM-PK-K6670)
13	Tropidostoma microtrema (SAM-PK-K6671)
	7 Diictodon galeops (SAM-PK-K6672, K6675-K6680)
	Dicynodontia (SAM-PK-K6673)
	Pristerodon mackayi (SAM-PK-K6674)
14	Ictidosuchoides longiceps (SAM-PK-K6681)
	3 Diictodon galeops (SAM-PK-K6682-K6684)
15	5 Diictodon galeops SAM-PK-K6685, K6687, K6688, K6690, K6691)
	Pristerodon mackayi (SAM-PK-K6686)
	Dicynodontia (SAM-PK-K6689)
	Oudenodon baini (SAM-PK-K6692)
16	Charassognathus gracilis gen. et sp. nov. (SAM-PK-K10369)

DESCRIPTION

The skull is complete and well preserved, albeit laterally compressed (Fig. 3A). The snout is slightly shorter (23 mm) than the temporal region (26 mm), which differs from therocephalians and other Late Permian cynodonts (e.g. Procynosuchus and Nanictosaurus) in which the snout is longer than the temporal region. The latter condition is observed even in juvenile Procynosuchus specimens.

The left premaxilla is absent and incompletely preserved on the right side of the snout. The facial process of the septomaxilla is anteroposteriorly wide, a condition that contrasts with that seen in other cynodonts, but is observed in various therocephalians (e.g. Ictidosuchops: BP/1/218, Glanosuchus: Van den Heever, 1994: fig. 1). Two upper incisors are present on the right side interdigiting with the lower incisors. The preserved incisors are interpreted as the second and fourth uppers and the first and third lowers (Fig. 3B). The portion of premaxilla that is not preserved is assumed to have lodged one more upper tooth. Four upper and three lower incisors is a condition widely distributed in many cynodonts, including most of the South African Late Permian forms. Precanines are absent and instead a diastema between the last incisor and the canine is present and accommodates the lower canine. Absence of precanines is common in most cynodonts apart from Procynosuchus and Dvinia (Tatarinov, 1968; Kemp, 1979).

The maxilla accommodates a large upper canine and seven postcanines. There is a space between the upper canine and the first postcanine on each side of the jaw, suggesting that another postcanine was lodged here (an alveolus is present on the right side). The canines are proportionately larger than those of Procynosuchus specimens of equivalent size. The two anteriormost postcanines are simple and lack accessory cusps, whereas the succeeding postcanines have a high main cusp and tiny anterior and posterior accessory cusps. These accessory cusps are similar in size, although the anterior accessory cusps are located slightly higher on the crown than the posterior accessory cusps. The main cusps of the postcanines decrease in height towards the back of the tooth row. There are two and three lower postcanines preserved on the right and left sides, respectively. The postcanines in Charassognathus differ from those of most therocephalians, which usually have a single cusp. However, at least two therocephalians are known to exhibit a more complex crown in the postcanines: the accessory cusps of Scaloporhinus angulorugatus (Mendrez, 1967) are virtually indistinguishable from the main cusp in lateral view, whereas the central and accessory cusps of Ericiolacerta parva are similarly developed (Crompton, 1962). The therocephalian Bauria also shows a more complex postcanine crown pattern, but only one cusp can be seen in labial view (Crompton, 1962; King, 1996). The morphology of the posterior postcanines of Charassognathus in labial view is most similar to that of Nanictosaurus (Van Heerden, 1976; Van Heerden & Rubidge, 1990), although the latter genus has more prominent accessory cusps that are more strongly differentiated than those on the first postcanine, whereas accessory cusps are absent on the first postcanine of Charassognathus.

The nasal extends along the dorsal surface of the snout and contacts the lacrimal, whereas the prefrontal forms the antero-dorsal border of the orbit and contacts the nasal, lacrimal and postorbital. In addition, as is typical in cynodonts, the frontal is excluded from the orbital margin by the prefrontal and postorbital. The parietal appears to be similar to that of other cynodonts, forming a conspicuous sagittal crest, which is broken anteriorly but forms a well-defined sharp crest posteriorly. The parietal foramen is located in the middle of the extension of the sagittal crest (approximately two-thirds along the length of the parietal). The parietal bones are fused behind the parietal foramen as in Cynosaurus, Progalesaurus and Galesaurus (Sidor & Smith, 2004).

The epipterygoid is visible in lateral view and contacts the parietal dorsally and the prootic posteriorly. The dorsal margin shows that the ascending process was anteroposteriorly extended as in all cynodonts and differs from the condition present in most therocephalians (apart from Theriognathus).

The jugal contacts the lacrimal and maxilla anteriorly and forms a posterolaterally orientated suture with the maxilla, similar to other basal cynodonts. The squamosal forms the posterior portion of the zygomatic arch, but it is not possible to recognize sutures in the posterior portion of the jugal. On the posterior surface of the temporal fenestra the squamosal deepens posteriorly and contacts the parietal dorsally. In occipital view the squamosal has a deep groove in the shape of an inverted ‘V’ for the quadratojugal. This groove is deeper and more prominent than that seen in Procynosuchus. A well-developed, although deformed, right occipital condyle is observed in the occipital plate, and dorsal to it there is a small protuberance, which is common in cynodonts and is generally interpreted as an articulation for the proatlas (e.g. Romer, 1969). Owing to the lateral compression of the skull, the palatal region could not be observed. The ascending process of the epipterygoid was anteroposteriorly extended, as in all cynodonts.

The lower jaw features of Charassognathus, including the deep, robust horizontal rami, the angle of the dentary and the anteroposteriorly extended coronoid process, resemble that of other cynodonts. The mandibular symphysis, as is typical of basal cynodonts, is unfused. The angle of the dentary in Charassognathus is clearly more prominent than in Dvinia and Procynosuchus. A small notch is present on the dentary (3, 4), at the base of the coronoid process, in a similar position to where the base of the masseteric fossa is located in Dvinia and Procynosuchus. A small (approximately 3.6 mm in length), oblong opening is present between the dentary and the angular, posterior to the notch of the dentary. This opening is also known in several therocephalians and in some basal cynodonts (see Brink, 1965c: fig. 49B; Kemp 1979: fig. 6a), although it is usually more developed than what is seen in Charassognathus. The angular is widely exposed laterally and, as is usual in basal cynodonts (including Thrinaxodon), the surangular forms a narrow strip of bone dorsal to the angular, which overhangs the latter bone in lateral view. The partially preserved reflected lamina of the angular is an osseous plate with some indication of lateral crests and corrugation, but appears less developed than in therocephalians, and is closer to the morphology of Procynosuchus and galesaurids.

The axis is articulated with the third cervical vertebra and they are both located on the occipital plate, displaced from their original position. The left side of the fused atlas centrum is visible and shows a large convex area, which is orientated anteriorly. This area is not well preserved, and the articular facets for the atlas arches and intercentrum, as described in Procynosuchus and galesaurids (Jenkins, 1971; Kemp, 1980), cannot be recognized. The transverse process of the axis is slightly larger than that of the third cervical vertebra and is more vertically orientated. The latter condition contrasts that reported and illustrated in Galesaurus in which the transverse process of the atlas is more horizontally orientated than the processes of the remaining cervical vertebrae (Jenkins, 1971). The postzygapophysis of the axis and the prezygapophysis of the third cervical are subvertically orientated. In contrast to Thrinaxodon and Galesaurus (Jenkins, 1971), there is no anapophysis in the axis of Charassognathus. A flattened bone, approximately rectangular and slightly curved dorso-ventrally, is preserved close to the transverse process of the axis. This bone is tentatively interpreted as a cervical rib.

The femur, tibia and fibula are all approximately equal in length. The femoral diaphysis is short and robust and the head is set off dorsally to the shaft of the bone (Fig. 3C). This last feature is similar to the cynodont condition (Jenkins, 1971) and differs from that in therocephalians (Kemp, 1986) in which the femoral head is directed mostly inward towards the acetabulum.

DISCUSSION

The existence of at least six species of Late Permian cynodonts, together with their widespread distribution in Gondwana (South Africa, Zambia and Tanzania) and Laurasia (Germany and Russia), is a clear indication that cynodonts were already in a first phase of diversification at this stage. Procynosuchus is generally regarded as the earliest cynodont, and ranges through the entire Dicynodon AZ in South Africa (Sidor & Smith, 2004) and coeval beds in East Africa and Europe. However, the holotype of Scalopocynodon gracilis (Brink, 1961), which was synonymized to Procynosuchus delaharpeae by Hopson & Kitching (1972), was recovered from the uppermost portion of the Cistecephalus Zone of Kitching (1977), which corresponds to the Cistecephalus AZ of Rubidge (1995). The presence of Procynosuchus in the Cistecephalus AZ is confirmed by the recent collection of specimens (SAM-PK-K8511 and PK-K10395, collected by R. Smith) from the uppermost portion of the Cistecephalus AZ in the Karoo Basin that are referable to Procynosuchus. The discovery of Charassognathus in the Tropidostoma AZ significantly extends the range of Cynodontia further downwards into the early Late Permian. It also reduces the extensive ghost lineage for the Cynodontia, when considering that its putative sister group, the Therocephalia, appears in the Middle Permian Eodicynodon AZ (Rubidge, 1995).

A cladistic analysis with equally weighted characters resulted in nine most parsimonious trees (MPTs), with the strict consensus tree showing a polytomy of the basal cynodonts: Charassognathus, Procynosuchus, Dvinia, and a clade including the remaining cynodonts. In the majority rule consensus (Fig. 5A), the basal polytomy decreases because Procynosuchus and Dvinia form a monophyletic clade in five of the nine MPTs. Cynosaurus follows the basal polytomy, and the other Late Permian cynodont, Nanictosaurus, appears as the sister taxon of the Early Triassic Thrinaxodon in the majority rule consensus tree (Fig. 5A). The analyses with implied weights with the different coefficients of concavity resulted in one MPT. The single MPT obtained from the analysis with the coefficient set at six (low value) is similar to one of the nine fundamental trees obtained from the previous analysis (Fig. 5B), whereas the MPT obtained with the coefficient set at three and one (stronger values) shows one difference in that Bauria and Ictidosuchops have swapped positions. In the trees obtained with implied weights Charassognathus is the most basal cynodont, followed by the clade [Procynosuchus, Dvinia] (Fig. 5B). Hopson & Kitching (2001) also obtained the latter clade as one of their MPTs, but it was not their preferred hypothesis. In agreement with the majority rule consensus with equally weighted characters, Thrinaxodon and Nanictosaurus are sister taxa in the MPTs in the analysis with implied weights. The latter relationship increases the number of cynodont lineages that crossed the Permo-Triassic boundary in the South African Karoo Basin from two (Sidor & Smith, 2004) to three (Fig. 6), implying that the cynodonts were the most successful therapsid group to survive the end-Permian extinction event.

Our results indicate that, contrary to all recent phylogenetic analyses that include several therocephalian taxa (Hopson & Barghusen, 1986; Van den Heever, 1994; Rubidge & Sidor, 2001), Therocephalia is paraphyletic (Fig. 5). Lycosuchus, usually considered to be a basal therocephalian (Van den Heever, 1994), is placed outside the majority of ‘therocephalians’ and the whaitsiid Theriognathus is placed as a sister taxon to the cynodonts, a hypothesis previously proposed by Kemp (1972a). Even when the placements of Lycosuchus, ‘Therocephalia’ and Theriognathus are poorly supported (Bremer Support = 1), the phylogeny presented here is the best hypothesis provided by our data. It is beyond the scope of the present study to analyse these results in detail. Further studies on the phylogenetic relationships of therocephalians will be addressed elsewhere.

The discovery of Charassognathus in the Tropidostoma AZ of South Africa and its basal placement in cynodont phylogeny indicates that the origin of this key therapsid group can be traced to the early Late Permian (Lopingian Epoch, Wuchiapingian Stage; Catuneanu et al., 2005) of the Karoo Basin in South Africa (Fig. 6). This finding differs from other recent phylogenies of the group (Hopson & Kitching, 2001; Sidor & Smith, 2004) where the Russian Dvinia was considered to be the most basal cynodont. The phylogenetic placement of Charassognathus in the MPTs obtained with implied weights (our preferred hypothesis) indicates that, contrary to general opinion (e.g. Hopson & Barghusen, 1986; Hopson & Kitching, 2001), four upper and three lower incisors, a condition that characterizes the majority of non-mammaliaform cynodonts (and also present in three of the four South African Late Permian taxa), was plesiomorphic in this group. Thus, the high number of upper and lower incisors and the presence of precanines (which are generally assumed to be plesiomorphic features in cynodonts) appeared later in cynodont evolution and are synapomorphies for the clade that includes Dvinia and Procynosuchus.

The lateral surface of the ramus mandibulae of the dentary is smooth in ‘therocephalians’, without any evidence of muscle attachment. The temporal fossa in this group is usually smaller than that in cynodonts (with Theriognathus possibly being the only exception) and the ramus mandibulae is placed laterally in the fossa, close to the zygomatic arch of the skull. This kind of arrangement leaves no room for the accommodation of the adductor muscles between the dentary and the zygoma (Barghusen, 1968). The dentary notch of Charassognathus is the first evidence of changes occurring on the lateral side of the ramus mandibulae in eutheriodonts. Considering the similar location of the dentary notch of Charassognathus and the base of the masseteric fossa in Procynosuchus and Dvinia, we interpret this notch as related to the invasion of adductor mandibulae externus musculature on the lateral surface of the dentary. A rapid evolution of the masseter insertion area occurred in the latest Late Permian, with two successive stages: (1) the development of a masseteric fossa in Procynosuchus and Dvinia, with its base having a similar location to the notch in Charassognathus, and (2) an extension of the masseteric fossa to the base of the dentary in Cynosaurus and Nanictosaurus. The location of the masseteric fossa high on the coronoid process in Procynosuchus was interpreted as an initial stage in the differentiation of the masseter, which was then followed by the extension of its insertion, reaching the angular region of the dentary (Barghusen, 1968; Bramble, 1978; but see Kemp, 1979, for a different interpretation of masseter evolution).