Garjainia prima, AND ITS

DIAGNOSIS OF GARJAINIA PRIMA AND ITS SYNONYMY WITH ‘ GARJAINIA TRIPLICOSTATA’

The genus Garjainia can be distinguished from other erythrosuchids based on multiple character states (see Diagnosis), several of them preserved in the holotype of Garjainia prima . The general morphology of the holotype of Garjainia prima is very similar to the hypodigm of Garjainia madiba despite the large geographical distance separating them, the former being known from European Russia and the latter from South Africa ( Gower et al., 2014). The presence of such similar species in localities so distant from one another is consistent with the hypothesis of a high degree of global cosmopolitanism among tetrapod land assemblages during the Early Triassic ( Shishkin et al., 2006; Button et al., 2017). The distinction between the holotypes of Garjainia prima and Garjainia madiba is complicated by the low number of overlapping elements for direct comparison. However, the holotype of Garjainia prima differs from Garjainia madiba in possessing a premaxilla with a palatal process that is gently curved ventrally and five tooth positions, jugal and postorbital bones without ball-like bosses on their external surfaces, and a basioccipital with a median tuberosity on its ventral surface (see also Gower et al., 2014).

The erythrosuchid ‘ Vjushkovia triplicostata ’ had historically been considered as closely related to or a subjective junior synonym of Garjainia prima ( Gower & Sennikov, 2000) . The specimens that form the hypodigm of ‘ Vjushkovia triplicostata ’ share with the holotype of Garjainia prima and /or the hypodigm of Garjainia madiba , but not with other erythrosuchids, the presence of a longitudinal groove on the lateral surface of the premaxillary body, basioccipital with basal tubera clearly separated from each other, anterior and middle postaxial cervical vertebrae with a distinct longitudinal lamina extending along the lateral surface of the centrum at mid-height, interclavicle with a rhomboidal posterior ramus, ilium with semicircular preacetabular process in lateral view, and pubis with prominent tuberosity for the attachment of the ambiens muscle in mature individuals. In addition, ‘ Vjushkovia triplicostata ’ shares with the holotype of Garjainia prima , but not with Garjainia madiba , the presence of a premaxilla with five tooth positions, jugal without a ball-like boss on its external surface, and basioccipital with a median tuberosity on its ventral surface. As a result, ‘ Vjushkovia triplicostata ’ is more similar to the holotype of Garjainia prima than to any other described taxon.

The morphology of the holotype of Garjainia prima is mostly identical to that of the hypodigm of ‘ Vjushkovia triplicostata ’, but the two differ in that the former specimen lacks palatal teeth on the palatine and pterygoid and possesses a completely thecodont tooth implantation. These two character states have been shown to be informative in several phylogenetic analyses focused on non-archosaurian archosauromorphs, including the present one, and may support a species-level distinction between Garjainia prima and ‘ Vjushkovia triplicostata ’. However, the extremely similar overall morphology of these two nominal species means that these two potentially distinguishing characters might be intraspecifically variable in this case. The Permian and Triassic archosauromorphs that we have examined at first hand do not show intraspecific variation in the presence or absence of palatal teeth, but assessing variation in this character is complicated by the very small number of individuals sampled for the vast majority of these species. Additionally, the presence of palatal teeth is intraspecifically variable in several species of extant iguanid, teiid, lacertid, scincid, anguid, helodermatid, boid and colubrid lepidosaurs ( Mahler & Kearney, 2006).

Regarding the difference in tooth implantation, the condition of this character is difficult to determine in some non-archosaurian archosauromorphs. For example, in the holotype of the Early Triassic proterosuchid ‘ Chasmatosaurus ’ yuani there is a single tooth ankylosed to the bone, whereas all other teeth are not ankylosed (IVPP V36315 View Materials ). Gower et al. (2014: 18) noted that in Garjainia madiba ‘the instances of close bonetooth association are not prevalent or strongly developed enough for the implantation as a whole to be considered ankylothecodont, and the dentition is overall more thecodont than in, for example, Proterosuchus and Sarmatosuchus ’. Within Erythrosuchidae, Middle Triassic species (e.g. Erythrosuchus africanus , Shansisuchus shansisuchus ) possess a completely thecodont tooth implantation, whereas early erythrosuchids retain an ankylothecodont condition (e.g. Guchengosuchus shiguaiensis ) ( Ezcurra, 2016). Thus, it is possible that the genus Garjainia shows an intermediate condition, with a perhaps relictual ankylothecodont condition in some individuals and a polymorphic tooth implantation in others, before thecodonty finally fixed in the phenotype of Middle Triassic erythrosuchids.

In conclusion, we consider here (in agreement with Gower & Sennikov, 2000) that ‘ Vjuskovia ’ and ‘ Vjushkovia triplicostata ’ are junior synonyms of Garjainia and Garjainia prima , respectively, based on the observation in other diapsids of intraspecific variability in the characters that differ between them and the unique combination of character states that they share among Permian and Triassic archosauromorphs.

THE PHYLOGENETIC RELATIONSHIPS OF THE ERYTHROSUCHIDS

Garjainia prima has been considered to be closely related to the South African species Erythrosuchus africanus and, therefore, within the family Erythrosuchidae , ever since the former species was erected in the late 1950s. The earliest quantitative phylogenetic analysis that focused on erythrosuchids ( Parrish, 1992) found Garjainia prima as the sister taxon of a clade composed of Erythrosuchus africanus , the Chinese Shansisuchus shansisuchus and the Russian ‘ Vjushkovia triplicostata ’ ( Parrish, 1992) . However, the latter species is considered here and by several previous authors (e.g. Gower & Sennikov, 2000; Gower et al., 2014; Ezcurra, 2016) as a junior synonym of Garjainia prima . More recently, ‘ Vjushkovia triplicostata ’ was recovered as more closely related to Erythrosuchus africanus than to Shansisuchus shansisuchus ( Ezcurra et al., 2010) . The phylogenetic analysis of Ezcurra (2016), which scored Garjainia prima based on the holotype and referred specimens of the species (i.e. including the hypodigm of ‘ Vjushkovia triplicostata ’), recovered Garjainia prima as the sister taxon of the clade composed of Erythrosuchus africanus , Shansisuchus shansisuchus and the Russian Chalishevia cothurnata , thus being more in agreement with the results of Gower & Sennikov (1996: analysis of braincase data only) than Parrish (1992).

Our analysis recovered the same phylogenetic interrelationships among erythrosuchids as Ezcurra (2016), with the exception of the position of Fugusuchus hejiapanensis as sister to all other members of Erythrosuchidae [this family is defined as a stem-based clade that includes all taxa more closely related to Erythrosuchus africanus Broom, 1905 than to Proterosuchus fergusi Broom, 1903 or Passer domesticus Linnaeus, 1758 sensu Ezcurra et al. (2010) ; therefore, Fugusuchus hejiapanensis lies within Erythrosuchidae ; Fig. 23 View Figure 23 ]. The phylogenetic position of the latter species at the base of Erythrosuchidae was also recovered by Parrish (1992), but contrasts with the results of Gower & Sennikov (1996, 1997), where Fugusuchus hejiapanensis was found as a proterosuchid.

The following unambiguous synapomorphies of Erythrosuchidae , which support the position of Fugusuchus hejiapanensis within the clade, are optimized in our analysis: postorbital with a lateral boss adjacent to orbital margin (128: 0→1; Fig. 23B–D View Figure 23 ), supraoccipital excluded from the dorsal border of the foramen magnum (209: 1→0), exoccipital with one foramen for the passage of the hypoglossal cranial nerve (222: 0→1), nasal with small lateral process that excludes the anteriormost tip of the prefrontal from the lateral margin of the skull roof (691: 0→1; Fig. 23B, C View Figure 23 ), postfrontal–postorbital suture mainly longitudinal in dorsal view, with an angle of ≥ 45° to the transverse axis of the skull (692: 0→1), and inferior and superior anterior processes of prootic closely approaching or joining together to form most or the anterior border of the foramen for the trigeminal cranial nerve (694: 0→1). It is interesting that none of these character states was found as a synapomorphy of Erythrosuchidae by Ezcurra (2016), showing that the position of Fugusuchus hejiapanensis at the base of the clade strongly modifies the ancestral synapomorphies of Erythrosuchidae . Branch support for Erythrosuchidae is low, with a minimal Bremer support and absolute and GC bootstrap frequencies of 21 and 4%, respectively.

In our analysis, the clade that includes Guchengosuchus shiguaiensis , Garjainia spp. , Erythrosuchus africanus , Shansisuchus shansisuchus and Chalishevia cothurnata possesses the following unambiguous synapomorphies: maxilla with neurovascular foramina lateroventrally facing and extending ventrally as deep, well-defined grooves on the lateral surface of the anterior and horizontal processes (53: 0→1), maxillary alveolar margin distinctly upturned in the anterior third of the bone (70: 0→1), parietal with a strongly transversely convex dorsal margin of the posterolateral process, which is elevated from the median line of the posterior margin of the skull roof (169: 0→1), and distal end of the radius strongly anteroposteriorly expanded (438: 0→1). All the above mentioned character states were optimized as synapomorphies of Erythrosuchidae by Ezcurra (2016), but the first one was recovered as a synapomorphy of the clade in only some trees. The Bremer support of this branch is minimal, but the bootstrap frequencies are considerably higher than those of Erythrosuchidae , with absolute and GC frequencies of 50 and 45%, respectively. These bootstrap frequencies are higher than those calculated for the same branch in the analysis of Ezcurra (2016).

The clade that includes Garjainia spp. , Erythrosuchus africanus , Shansisuchus shansisuchus and Chalishevia cothurnata is supported by the following unambiguous synapomorphies: maxillo-nasal tuberosity delimiting anteriorly the antorbital fossa (46: 0→1; Fig. 23C, D View Figure 23 ), maxilla with an antorbital fossa on the lateral surface of the bone (54: 0→1), anterior margin of the base of the ascending process of the maxilla subvertical (58: 1→2), edentulous anterior portion of the ventral margin of the maxilla (69: 0→1), ventral surface of the frontal with a median longitudinal canal for the passage of the olfactory tract only slightly constricted and without olfactory bulb impressions and distinct semilunate posteromedially to anterolaterally oriented ridges on the orbital roof (120: 0→1), pineal fossa on the midline of the dorsal surface of the parietal (162: 0→1), lateral surface of the surangular with a laterally projecting shelf that possesses a strongly convex lateral edge (286: 2→3), anterior cervical vertebrae with a median longitudinal keel on the ventral surface of the centrum that extends ventral to the centrum rim in at least one vertebra (327: 1→2), postaxial cervical vertebrae with a shallow, posterolaterally facing fossa on the posterior portion of the neural arch ventral to the postzygapophysis (335: 0→1), and articular with a dorsomedial projection separated from glenoid fossa by a clear concave surface (652: 0→1). Characters 54 and 652 represent new synapomorphies added to those already recognized for this clade in the analysis of Ezcurra (2016). This branch is well supported, with a Bremer support of four and absolute and GC bootstrap frequencies of 86 and 84%, respectively, slightly higher support values than those in Ezcurra (2016).

In our analysis, Garjainia possesses the following unambiguous synapomorphies: supratemporal fossa immediately medial or anterior to the supratemporal fenestra on the dorsal surface of the skull roof (8: 0→1), premaxilla with a longitudinal groove placed approximately at mid-height and extending along most of the length of the lateral surface of the main body of the bone (31: 0→1), quadrate medial condyle distinctly more distally projected than the lateral one (183: 0→1), opisthotic with fossa immediately lateral to the foramen magnum on the occipital surface (216: 0→1), basioccipital with basal tubera clearly separated from each other (227: 1→0), anterior and middle postaxial cervical vertebrae with a distinct longitudinal lamina extending along the lateral surface of the centrum at mid-height (340: 0→1), ilium with semicircular preacetabular process in lateral view (461: 1→0), and pubis with prominent tuberosity for the attachment of the ambiens muscle in mature individuals (474: 1→0; also proposed as apomorphic for Garjainia by Gower et al., 2014). Ezcurra (2016) found a single unambiguous synapomorphy for Garjainia (character 8), whereas all the other synapomorphies were recovered in only some optimal trees. Here, the number of unambiguous apomorphies for Garjainia is greater because GHG 7433MI, a still undescribed small erythrosuchid specimen from the Cynognathus Assemblage Zone of South Africa (see Ezcurra, 2016), was not included in the analysis. GHG 7433MI possesses a high proportion of missing data that generated several ambiguous optimizations for the genus Garjainia in the results of Ezcurra (2016). As a result of the exclusion of this specimen, branch support for Garjainia is greater than found by Ezcurra (2016), with a Bremer support of three and absolute and GC bootstrap frequencies of 85 and 79%, respectively.

The clade comprising the Middle Triassic erythrosuchids Erythrosuchus africanus , Shansisuchus shansisuchus and Chalishevia cothurnata has the following unambiguous synapomorphies in our analysis: premaxilla with a peg on the posterior edge of the main body (33: 0→1), nasal contributing to the dorsal border of the antorbital fossa (83: 0→1), jugal with posterior process extending beyond the level of the infratemporal fenestra (106: 0→1), squamosal with sharp transition between the anterior and ventral processes and the posterodorsal border of the infratemporal fenestra acquires a square outline (139: 1→0), squamosal with ventral process forming almost the entire posterior border of the infratemporal fenestra (146: 1→2), squamosal with a posterodorsally to anteroventrally oriented tuck on the lateral surface of the ventral process (147: 0→1), opisthotic with ventral ramus covered by the lateralmost edge of the exoccipital in posterior view (218: 0→1), exoccipital with distal end contacting its counterpart along the entire dorsal surface of the basioccipital, excluding the basioccipital from the floor of the endocranial cavity and the dorsal surface of the occipital condyle (221: 1→2), braincase without pseudolagenar recess (223: 0→1), parabasisphenoid with base of the cultriform process tall, with the dorsal edge extending between the clinoid processes and the ventral part of the crista prootica (243: 0→1), external foramina for the passage of the abducens nerves (cranial nerve VI) open anteriorly (251: 1→0), prootic with a ridge on the lateral surface of the inferior anterior process ventral to the trigeminal foramen (256: 0→1), dentary with mostly straight tooth-bearing portion (267: 1→0), cervico-dorsal transition with a very strong anteroposterior compression of the centra, being considerably anteroposteriorly shorter than tall (311: 0→1), ulna with lateral tuber (= radius tuber) on the proximal portion (433: 0→1), calcaneum with an expanded distal end of the calcaneal tuber in proximal or distal view (549: 0→1), ilium with subtriangular, tapering posteriorly postacetabular process in lateral view (688: 0→1), and premaxilla with distinctly convex alveolar margin in lateral view (690: 0→1). Characters 139, 433, 688 and 690 are newly identified synapomorphies for this clade found in our analysis. The Bremer support of this clade is two, and the bootstrap absolute and GC frequencies are 68 and 58%, respectively, being slightly higher than those recovered by Ezcurra (2016).

The clade composed of Shansisuchus shansisuchus and Chalishevia cothurnata possesses the same two synapomorphies found by Ezcurra (2016): secondary antorbital fenestra immediately anterior to the antorbital fenestra (15: 0→1), and postaxial cervical vertebrae without excavation immediately lateral to the base of the neural spine (337: 1→0). The branch supports calculated here for this clade are very similar to those of Ezcurra (2016), with a Bremer support of one and bootstrap absolute and GC frequencies of 61 and 33%, respectively.

Suboptimal searches constraining the position of Garjainia prima in different positions of the tree found that 28 additional steps are necessary to force its placement as an eucrocopod, 16 to be sister to all other erythrosuchids, 12 extra steps to be the sister taxon of Erythrosuchus africanus , and ten to be the sister taxon of Fugusuchus hejiapanensis , Guchengosuchus shiguaiensis and Shansisuchus shansisuchus . The floating taxon Garjainia madiba was found as the sister taxon of Garjainia prima in all these suboptimal searches. Thus, the phylogenetic position of Erythrosuchus africanus as more closely related to Garjainia prima than to Shansisuchus shansisuchus proposed by Ezcurra et al. (2010) is very poorly supported in the context of the current data set.

Regarding Fugusuchus hejiapanensis , three additional steps are necessary to recover this species in the same position as found by Ezcurra (2016), four steps to be the sister taxon of Sarmatosuchus otschevi , Guchengosuchus shiguaiensis or of all the other erythrosuchids with exception of Guchengosuchus shiguaiensis , five steps to force its placement as a proterosuchid, and six steps to be the sister taxon of Archosauriformes. As a result, the phylogenetic position of Fugusuchus hejiapanensis as an erythrosuchid is moderately supported by our data set.

The bootstrap GC frequencies calculated under implied weights are lower than those under equal weights for the entire range of used k values (3–18) in Proterosuchidae and the clade that includes Sarmatosuchus otschevi and more crownward archosauriforms, and Erythrosuchidae . The condition is similar for Erythrosuchidae , but with k values of 15 and 18 the frequencies are slightly higher under implied weights. In the case of the genus Garjainia , k values between three and eight recovered lower frequencies than those under equal weights, whereas using higher k values the frequencies were higher. In contrast, the clade comprising Erythrosuchus africanus , Shansisuchus shansisuchus and Chalishevia cothurnata possesses higher GC frequencies under implied weights than using equal weights, with exception of the extreme condition of a k constant equal to three. As a result, weighting against homoplasy reduces the resampling support for higher-level clades among ‘proterosuchians’, indicating that characters with high levels of homoplasy contribute substantially to the monophyly of these groups. The condition is intermediate for the genus Garjainia , in which moderately low weighting produces a better supported branch. The clade that comprises Middle Triassic erythrosuchids is supported by characters with low homoplasy and, as a result, implied weights increase its support. These results indicate that the morphology of Middle Triassic erythrosuchids was specialized in ways not generally explored by other Triassic archosauromorphs.

CONCLUSIONS

The holotype of Garjainia prima possesses a unique combination of character states that allow it to be distinguished from other Triassic archosauromorphs, including its sister species, Garjainia madiba . These character states, and the absence of substantial evidence supporting the taxonomic distinctiveness of ‘ Vjushkovia triplicostata ’, bolster the hypothesis that the latter species is a subjective junior synonym of Garjainia prima . The genus Garjainia is placed as the sister taxon of Middle Triassic erythrosuchids, the latter showing a series of apomorphies with low degrees of homoplasy. Thus, Middle Triassic erythrosuchids acquired morphologies rarely explored by other early archosauromorphs. Our revision of the anatomy of Garjainia prima allowed us to identify phylogenetically informative characters that were used to expand a previously published phylogenetic data set focused on Permo-Triassic archosauromorphs. The modifications of this data set resulted in the recovery of Fugusuchus hejiapanensis from the upper Lower Triassic of China as sister to all other erythrosuchids, rather than as outside of the clade composed of Erythrosuchidae + Eucrocopoda that was recovered by previous analyses. This new phylogenetic hypothesis resulted in a modification of the unambiguous ancestral synapomorphies of Erythrosuchidae .