The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of Caecilians

Abstract

The scant fossil record of caecilians has obscured the origin and evolution of this lissamphibian group. Eocaecilia micropodia from the Lower Jurassic of North America remains the only stem-group caecilian with an almost complete skull preserved. However, this taxon has been controversial, engendering re-evaluation of traits considered to be plesiomorphic for extant caecilians. Both the validity of the placement of E. micropodia as a stem caecilian and estimates of the plesiomorphic condition of extant caecilians have been questioned. In order to address these issues, the braincase of E. micropodia was examined via micro-computed tomography. The braincase is considered to be a more reliable phylogenetic indicator than peripheral regions of the skull. These data reveal significant new information, including the possession of an ossified nasal septum, ossified anterior wall of the sphenethmoid, long anterolateral processes on the sphenethmoid, and paired olfactory nerve foramina, which are known only to occur in extant caecilians; the latter are possibly related to the evolution of the tentacle, a caecilian autapomorphy. A phylogenetic analysis that included 64 non-amniote taxa and 308 characters represents the first extensive test of the phylogenetic affinities of E. micropodia. The results place E. micropodia securely on the stem of extant caecilians, representing a clade within Temnospondyli that is the sister taxon to batrachians plus Gerobatrachus. Ancestral character state reconstruction confirms the braincase of E. micropodia to be largely representative of the plesiomorphic condition of extant caecilians. Additionally, the results refine the context within which the evolution of the caecilian form can be evaluated. The robust construction and pattern of the dermal skull of E. micropodia is interpreted as symplesiomorphic with advanced dissorophoid temnospondyls, rather than being autapomorphic in its robust construction. Together these data increase confidence in incorporating E. micropodia into discussions of caecilian evolution.

Figure 1. Volume rendering of the µCT data of the holotype of Eocaecilia micropodia (MNA V8066).

A, dorsal view. B, ventral view.

Figure 2. The braincase and middle ear ossicle of Eocaecilia micropodia as revealed by µCT.

A–C, three-dimensional digitally segmented braincase of the holotype (MNA V8066) in dorsal, left lateral and ventral views, respectively, with the sphenethmoid (orange) and the os basale (blue). D–E, surface renderings of an isolated braincase referred to E. micropodia (MNA V8063) in dorsal and ventral views, respectively. The alternative hypotheses of foramen identity are depicted in blue and green. F–H, three-dimensional digitally segmented middle ear ossicle of E. micropodia (MNA V8066) in dorsal, left lateral, and ventral views respectively. This element is termed the stapes-quadrate by Jenkins et al. because of the hypothesized fusion of these two elements. Abbreviations: ant., antotic region; ant.w., antotic wall; a.l.p., anterolateral process; d.s., dorsal surface of the otic capsule; f.c.a., foramen for the carotid artery; f.d.v., foramen for a dorsal vein; f.j., jugular foramen; f.s., stapedial foramen; f.v., fenestra vestibuli; f.1, foramen 1 (see text for interpretation); f.2, foramen 2 (see text for interpretation), f.V_mx,md, foramen for the maxillary plus mandibular trunk of the trigeminal nerve; f.V_op, foramen for the ophthalmic branch of the trigeminal nerve; n.s., nasal septum; oto., otic-occipital complex; o.ca., otic capsule.

Figure 3. Identification of paired dorsal and ventral foramina, serving the likely transmission of the paired trunks of the olfactory nerve, similar to the condition seen in extant caecilians.

A, µCT image of a transverse section through the level of the anterior sphenethmoid in E. micropodia (MNA V8066), showing the location of dorsal and ventral foramina in the anterior wall of the sphenethmoid. B, posterior view of the three-dimensionally segmented sphenethmoid of E. micropodia, further showing the locations of the anterior foramina interpreted here as those serving the dorsal and ventral trunks of the olfactory nerve. C, posterior view of the three-dimensionally segmented sphenethmoid of the extant caecilian Dermophis mexicanus (UMMZ 219030), showing the location of comparable foramina known to transmit the trunks of the olfactory nerve . Abbreviation: f.I_D, foramen for the dorsal branch of the olfactory nerve; f.I_V, foramen for the ventral branch of the olfactory nerve.

Figure 4. The 50% majority-rule consensus tree of the 34 most parsimonious trees obtained in the parsimony analysis (1450 steps).

Numbers above nodes represent bootstrap values greater than 50% (values below 50% not shown). Within the temnospondyl lineage a monophyletic Lissamphibia was obtained. Eocaecilia micropodia was recovered on the stem of extant caecilians (Apoda) and together this clade (Gymnophiona) formed the sister taxon to the clade of Batrachia plus Gerobatrachus. The sister taxon to Lissamphibia in this hypothesis is Doleserpeton.

Figure 5. Alternative hypotheses for the evolution of the open temporal region in extant lissamphibians.

A, Scenario in which the open condition is homologous for lissamphibians, and Eocaecilia micropodia is a homoplastic reversal to the condition present in Doleserpeton. B, Scenario in which the open condition is a homoplastic convergence between extant caecilians and batrachians plus Gerobatrachus. This hypothesis is favoured here given the occurrence of a similar condition in lysorophian lepospondyls. Illustrations modified from: Amphibamus ; Doleserpeton ; Eocaecilia ; caecilians ; Gerobatrachus ; frogs ; Triadobatrachus ; salamanders ; Karaurus .