Evolution of the MC in Crocodyliformes

The origins of Crocodyliformes and Mesoeucrocodylia are associated with an extensive reorganization of the temporal region of the skull (Whetstone & Whybrow, 1983; Clark, 1994; Clark et al. 2000, 2004; Holliday & Witmer, 2009; Pol et al. 2013). The hearing apparatus of extant crocodyliforms is unique among amniotes and includes a well‐developed external ear, something only present elsewhere in mammals. However, comparatively little effort has been made to investigate the anatomy of these structures and their evolutionary origins (Shute & Bellairs, 1955; Wever, 1978; Saunders et al. 2000; Vergne et al. 2009). The review of crocodyliform posterior skulls and osteological proxies of associated soft tissue structures of the ear map a complex pattern of evolution (Fig. 9).

Figure 9 Open in figure viewer PowerPoint Simplified phylogenetic framework with major stages in the evolution of the MC of Crocodyliformes discussed in the text. BOA, bony otic aperture; DOI, dorsal otic incisure; EAM, external auditory meatus; IOC, incisure of the otic aperture of the cranioquadrate passage; MC, meatal chamber; SF, subtympanic foramen.

The early forms, Protosuchus haughtoni, Hemiprotosuchus leali, Orthosuchus strombergi and Fruitachampsa callisoni, present the ancestral state of the MC in crocodyliforms. The broad, lateral expansions of the skull roof overhanging the temporal region in most crocodyliforms represents a plesiomorphy, present in a much broader phylogenetic assemblage, possibly at the base of Crocodylomorpha (Pol et al. 2013). A similar anatomy is also present in the paraphyletic array of closely related forms, such as Litargosuchus leptorhynchus (Clark & Sues, 2002; BP/1/5237), Pseudhesperosuchus jachaleri (Bonaparte, 1969), Hesperosuchus agilis (Colbert, 1952), Saltoposuchus connectens (von Huene, 1921), Terrestrisuchus gracilis (Crush, 1984), Dibothrosuchus elaphros (Simmons, 1965), Sphenosuchus acutus (Haughton, 1915), Kayentasuchus walkeri (Clark & Sues, 2002), Junggarsuchus sloani (Clark et al. 2004) and Almadasuchus figarii (Clark et al. 2000, 2004; Clark & Sues, 2002; Pol et al. 2013).

In addition, the sulcus on the outer surface of the squamosal and postorbital for the attachment of the upper earlid is also present in Kayentasuchus walkeri (Clark & Sues, 2002; Clark et al. 2004; Pol et al. 2013). Kayentasuchus walkeri has a variable position among Crocodylomorpha, recovered in a basal position in most topologies (Clark & Sues, 2002; Sues et al. 2003; Clark et al. 2004; Pol et al. 2013; Wilberg, 2015b), but also as a sister group of Crocodyliformes (Nesbitt, 2011) or as a basal member of that clade (Jouve, 2009). If future work confirms the basal position of Kayentasuchus walkeri outside Crocodyliformes, it implies that the muscular upper earlid was homoplastically acquired twice during the Crocodylomorpha evolution, once by Kayentasuchus walkeri and once at the Crocodyliformes node. Also, the recently described Almadasuchus figarii might have the sulcus for an upper earlid taphonomically obscured (Pol et al. 2013). If confirmed, the upper earlid represents a slightly more inclusive synapomorphy. The simultaneous occurrence of an inset BOA and the upper earlid bounding the MC laterally were already present at the origins of Crocodyliformes, as previous work has suggested (Nash, 1975; Hecht & Tarsitano, 1983; Busbey & Gow, 1984; Busbey, 1995; Gow, 2000; Clark & Sues, 2002; Clark et al. 2004; Pol et al. 2013).

The posteriorly opened MC, BOA and cranioquadrate passage present in the basal crocodylomorphs and other pseudosuchians, such as Terrestrisuchus gracilis, Dibothrosuchus elaphros and Sphenosuchus acutus (SAM PK K3014) presents the plesiomorphic state for Crocodyliformes (Walker, 1970; Clark et al. 2000, 2004; Benton & Walker, 2002; Nesbitt, 2011; Nesbitt et al. 2013; Pol et al. 2013; Butler et al. 2014a). The cranioquadrate passage is restricted between the quadrate and otoccipital early on, in non‐crocodyliform taxa such as Junggarsuchus and Almadasuchus, and persists throughout Crocodyliformes (Pol et al. 2013). The contact between the squamosal and the quadrate behind the MC occurred along the ‘protosuchian’ grade (Fig. 9). Some taxa do not have this region completely preserved, such as Fruitachampsa callisoni (LACM 120455a), Zosuchus davidsoni and Shantungosuchus hangjinensis, which hampers the complete understanding of the phylogenetic origin of this closure. Almadasuchus figarii may shed some support for a single, early origin of this closure, given the support for this taxon as a sister‐taxon to Crocodyliformes and the presence of a partially closed posterior MC (Pol et al. 2013), but see below alternative scenarios regarding Thalattosuchia. The closure is not as complete as that of Mesoeucrocodylia, and the posteroventrally downturned squamosal of this species differs greatly from that of mesoeucrocodylians. However, this anatomy suggests that at least a functional closure was present before Crocodyliformes and may have persisted throughout all protosuchians. The ‘protosuchians’ Protosuchus haughtoni, Hemiprotosuchus leali and Orthosuchus strombergi have more posteriorly open MCs than Almadasuchus. The squamosal in some of these taxa does bend posteroventrally, perhaps homologous to that of Almadasuchus, but the MC remains open posteriorly. Taxa closer to Mesoeucrocodylia, such as Hsisosuchus dashanpuensis (Gao, 2001) and Hsisosuchus chungkingensis (Young & Chow, 1953; Li et al. 1994; Gao, 2001), have fully closed posterior MCs as in extant crocodylians.

The BOA formed only by the EAM with the OI and lacking the OB, IOC and DOI exhibits very little change from its ancestral anatomy present in pseudosuchians (Benton & Clark, 1988; Benton & Walker, 2002; Nesbitt et al. 2009, 2013; Nesbitt, 2011; Butler et al. 2014a,b). On the other hand, the extra apertures, named quadrate fenestrae or quadrate foramina at the anterior perimeter of the OI, are uncommon and need a closer inspection for assessing the homology of its component across crocodyliforms. Another foramen, called the quadrate foramen, is commonly bounded between the quadrate and quadratojugal in archosauromorphs (Ewer, 1965; Sereno & Novas, 1992; Dilkes, 1998; Nesbitt et al. 2009; Nesbitt, 2011; Butler et al. 2014a,b). This foramen is closed at the origin of Crocodylomorpha (Benton & Clark, 1988; Nesbitt, 2011), but the same nomenclature has been applied to other quadrate structures within crocodylomorph ADQs (Walker, 1970; Busbey & Gow, 1984; Pol et al. 2013). Discussing the homology of the quadrate foramen across Archosauromorpha is beyond the scope of this paper. However, to avoid any implicit homology statement confusions, it is suggested to discard the term quadrate foramen for crocodylomorphs. The openings in the crocodylomorph ADQ are associated with the pneumatic diverticulae of the periotic sinus (Iordansky, 1973, Wever, 1978; Witmer, 1997; Hetherington, 2008; Montefeltro et al. 2011; Tahara & Larsson, 2011; Pol et al. 2014). In extant crocodylians, this diverticulum only exits the quadrate via the subtympanic foramen on the ADQ to return into the middle ear near the inner contact between the tympanum and quadrate. These openings are not covered in extant taxa and were probably uncovered in extinct taxa as well, and therefore should not be called fenestrae. In keeping with the preferred terminology, the multiple foramina in the ‘protosuchian’ ADQ are called here the subtympanic foramina. The presence of multiple subtympanic foramina is the plesiomorphic state for crocodyliforms and also presents two successive outgroups of the clade, Junggarsuchus sloani and Almadasuchus figarii (Clark et al. 2004; Pol et al. 2013). The number and configuration of these foramina is highly variable in crocodyliforms, and establishing the homology of each foramen across taxa is currently uncertain. However, a large subtympanic foramen, called fenestra ‘A’ by Hecht & Tarsitano (1983), seems to be a reliable landmark and is considered homologous in Protosuchus richardsoni, Protosuchus haughtoni, Orthosuchus strombergi, Fruitachampsa callisoni, Gobiosuchus kielanae, Shantungosuchus hangjinensis, Hsisosuchus dashanpuensis, Hsisosuchus chungkingensis and Hsisosuchus chowi. None of the basal crocodylomorphs has a putative subtympanic foramen ‘A’, and this structure on the ADQ might be an autapomorphy of crocodyliforms. The developed POF at the ADQ shows that the TM would have occupied a greater portion of the head in basal crocodyliforms even though the posterior limits of the membrane cannot be inferred from osteological correlates.

The phylogenetic context of the three MC patterns in basal mesoeucrocodylian indicates great modifications in this section of the crocodyliform evolutionary history (Fig. 9). The interpretation of the ancestral anatomy at this node is greatly biased by the discrepant ‘thalattosuchian pattern’ positioned in the primary phylogenetic framework as a basal Mesoeucrocodylia. In this scenario, a series of traits established in ‘protosuchians’ and present in other basal mesoeucrocodylian are absent or modified in this group. However, its alternative positions (Wilberg, 2015a,b) also imply a great amount of reversions and homoplasies to accommodate the interpretation of the ‘thalattosuchian pattern’ (see below).

The absence of the lateral shelves of skull roof over the MC in thallatosuchians and the absence of the longitudinal sulcus for the attachment of the upper earlid are unique traits among crocodyliforms. This anatomy represents a reversion from what is usually observed in basal Crocodylomorpha. It implies that in life, the TM in thalattosuchians was exposed and attached to the lateral edge of the head as in lizards and turtles today (Wever, 1978; Dooling et al. 2000; Werner et al. 2005; Christensen‐Dalsgaard & Carr, 2008; Christensen‐Dalsgaard et al. 2012; Willis et al. 2013).

The closure of the posterior portion of the MC and the otic aperture of the cranioquadrate canal occurred within the ‘protosuchian’ grade, and it is present in the ‘basal notosuchian/sebecian pattern’, the ‘advanced notosuchian pattern’ and plesiomorphically in neosuchians. In spite of the early advances in basal crocodyliforms to enclose the posterior MC, Thalattosuchia have a posteriorly opened MC, and a large but enclosed occipital aperture of the cranioquadrate passage. Accordingly, these modifications may have occurred as reversions to the plesiomorphic state, perhaps in association with reduced hearing function and a fully marine lifestyle. It is not clear if all basal thalattosuchians have the occipital aperture of the cranioquadrate passage enclosed by the quadrate, the squamosal and the otoccipital. However, the large clade of metriorhynchids certainly do (Fig. 5D). In addition, a closed occipital aperture of the cranioquadrate passage does not require the simultaneous occurrence of related structures as IOC and OB. In thalattosuchians, the posterior attachment of the TM did not occur in the suspensory plate or exhibit a different configuration not requiring an OB. Differently from other mesoeucrocodylians, the BOA represents the only aperture in the thalattosuchian ADQ, and implies an apomorphic state of the group, in which all the subtympanic foramina are closed.

The distribution of the ‘basal notosuchian/sebecian pattern’ along the phylogenetic framework shows this type of MC as the most widespread anatomy for the basal metasuchians (Fig. 9). During this section of the crocodyliform evolution, general traits were for the first time established and kept with minor subsequent changes along the later evolution of the group.

The inset BOA and longitudinal sulcus at the lateral edge of squamosal and postorbital (implying the presence of earlids) is ubiquitously present in metasuchians. This condition is shared with taxa with the ‘advanced notosuchian pattern’ and all neosuchians, including the crown‐group. In a similar way, the MC and BOA are closed posteriorly by the contact of the squamosal and the quadrate and the occipital aperture of the cranioquadrate passage closed by the quadrate, squamosal and the otoccipital.

The complex anatomy of the BOA, including the IOC, DOI and OB, is present for the first time in metasuchian, representing apomorphies for this group, and maintained in more derived forms. However, a closer inspection of the BOA anatomy of some ‘protosuchians’ (e.g. Hsisosuchus dashanpuensis and Hsisosuchus chungkingensis) can potentially change the interpretation for the origins of these structures. The presence of the IOC suggests that at the metasuchian node, the cranioquadrate passage becomes closer to the BOA, extensively enclosed in the canal formed laterally by the quadrate and squamosal, while the courses of the tempororbital vessels and seventh cranial nerve are closer to the condition of extant crocodyliforms (Benton & Clark, 1988; Sedlmayr, 2002). The dorsally displaced OB extends from the posterior wall of the BOA and restricts the IOC to a dorsal position (Fig. 6). It supports that the BOA was mostly covered by the TM in the ‘basal notosuchian/sebecian pattern’, which is different from the extant forms that have a greater portion of the BOA positioned posteriorly to the TM (Figs 2 and 3).

The subtympanic foramen is the only extra aperture in the ADQ of basal metasuchians with the ‘basal notosuchian/sebecian pattern’. The homology of this structure with one of the multiple apertures present in the ADQ of basal crocodyliforms and the ‘advanced notosuchian pattern’ was proposed. This proposition fulfils the homology criteria of similarity, conjunction and congruence (Patterson, 1982; Pinna, 1991), even though the variable configuration of the foramina discourages the assignment of the exact aperture that the subtympanic foramen is homologous to. However, the subtympanic ‘A’ (fenestra ‘A’) is not the best candidate given its posteroventral position at the margin of the OI, whereas the single subtympanic foramen of the ‘basal notosuchian/sebecian pattern’ is located anterodorsally to its equivalent position at the ADQ. The ventral margin of the POF suggests a complex morphology of the TM. This morphology might have been related to a unique shape for the TM different from the oval structure of the extant forms.

The greater modifications in ‘advanced notosuchian pattern’ are related to the extension of the sulcus at the lateral shelves of the skull for the upper earlid in baurusuchids, the dimensions of the MC, and the pattern of the multiple subtympanic foramina on the quadrate. The sulcus for the upper earlid in bauruschids suggests an orientation of the upper earlid that would have also expanded from the back of the MC, differently from the strictly vertical orientation from the skull roof in extant crocodyliforms and other fossil groups. The MC is dorsoventrally increased in ‘advanced notosuchian pattern’ due to a well‐developed postorbital descending flange, as in Pissarrachampsa sera (LPRP/USP‐0049), Notosuchus terrestris (MUCPv‐147), Mariliasuchus amarali (UFRJ DG 106‐R) and Caipirasuchus montealtensis (MPMA 15‐001/90). This is rather different from ‘protosuchians’ in which the expansion of the MC is achieved by a well‐developed anterodorsal process of the quadratojugal (e.g. Protosuchus haughtoni BP/1/4770).

The quadrate pneumatization in the ‘advanced notosuchian pattern’ is similar to the configuration of some of the basal crocodyliforms previously discussed, including the presence of a larger ventral‐most aperture in some taxa. The same discussion regarding the homology among the multiple extra apertures and the subtympanic foramen is valid here. Therefore, it is proposed that the structures called quadrate fenestrae in advanced notosuchians and baurusuchids are homologous to the single subtympanic foramina of the ‘basal notosuchian/sebecian pattern’, neosuchians, and ultimately to the multiple apertures in basal crocodyliforms. The phylogenetic distribution of the ‘advanced notosuchian pattern’ suggests an independent acquisition of the multiple pneumatic apertures from ‘basal notosuchian/sebecian pattern’. Thus, the direct homology among each of the extra subtympanic foramen in basal crocodyliforms and advanced notosuchians is not feasible. The unique orientation of the subtympanic foramina present in Baurusuchinae, in which most of the foramen are not facing laterally but perpendicularly to the BOA, creates a shelf at the anterior perimeter of the OI and a further inset BOA that ultimately works as a secondary BOA.

The taxonomical sampling was focused on basal Crocodyliformes, basal Mesoeucrocodylia and basal Metasuchia, in which the greater modifications in MC are concentrated. Accordingly, the current analysis did not embody the great diversity of fossil neosuchians, eusuchians and crocodylians. Further analyses with broader samples of neosuchians are desirable for a better understanding of the modifications in the MC of specific groups, such as dyrosaurids, goniopholidids and paralligatorids, as well as basal eusuchians and crocodylians.

The current analysis indicates that many characters of the MC in crown‐group Crocodylia were already established at the origins of Neosuchia. The neosuchian ADQ is ancestrally pierced by two apertures, the BOA and a single subtympanic foramen. The latter is absent in some forms and represents multiple evolutionary losses of this structure. The complex BOA including EAM, IOC and DOI is also the plesiomorphic state for the clade but the IOC assumes two anatomies among the neosuchians. The widespread condition is the same as described for ‘basal notosuchian/sebecian pattern’ and extant forms. It is present in an array of basal neosuchians and represents the plesiomorphic state for the clade.

The other condition is found in some derived groups of neosuchians in which the IOC assumes a unique morphology extending posteroventrally at the posteroventral corner of the BOA and forming a laterally and posteriorly opened cranioquadrate passage (Delfino et al. 2008). However, the configuration of the MC and BOA is achieved by secondary modifications of a typical neosuchian BOA. In these neosuchians, the squamosal is not limited to the skull roof and has a ventrally directed lamina bounding the MC and BOA posteriorly (Fig. 8C,E). The opened canal is formed dorsally by this squamosal lamina, ventrally by the quadrate, and posteromedially by the otoccipital. Anteriorly, the OB limits the canal as in neosuchians with closed cranioquadrate passage. Posteriorly, the otoccipital squamosal and quadrate fail to meet and enclose the occipital aperture of the passage.

The phylogeny of advanced neosuchians is in a state of flux. The hypotheses diverge in the position of neosuchians with secondarily opened cranioquadrate passage and there is no complete taxonomical overlapping among the hypotheses (Andrade et al. 2011; Buscalioni et al. 2011; Figueiredo et al. 2011; Adams, 2013, 2014; Montefeltro et al. 2013; Pritchard et al. 2013; Puértolas‐Pascual et al. 2014; Turner, 2015). In addition, key taxa, both in basal and derived positions in Neosuchia, lack well‐preserved MCs (e.g. Bernissartia fagesii; Dollo, 1883; IRScNBr 46; Theriosuchus pusillus; Owen, 1879; NHMUK 48330; Pholidosaurus purberckensis; NHMUK 36721). These circumstances preclude a detailed analysis of the changes in the morphology of the cranioquadrate passage along neosuchian evolutionary history. However, all hypotheses imply a closed cranioquadrate passage as the ancestral state for Neosuchia and Crocodylia, but not necessarily for Eusuchia, and also imply multiple shifts in this character along the evolutionary history of neosuchians (Delfino et al. 2008; Martin, 2010; Andrade et al. 2011; Brochu, 2011, 2012; Buscalioni et al. 2011; Figueiredo et al. 2011; Puértolas et al. 2011; Conrad et al. 2013; Puértolas‐Pascual et al. 2014; Turner, 2015).