Evolution of the Amphibian Ear with Implications for Lissamphibian Phylogeny: Insight Gained from the Caecilian Inner Ear

Abstract

The inner ear is a complex structure consisting of the vestibular and auditory systems. Across vertebrates, morphological variation in the inner ear provides a source of homologous features (characters) that may aid in resolving phylogenetic relationships. The morphology of the inner ear in extant frogs and salamanders is well known, and has been extensively studied from functional perspectives. However, the ability of its form and features to shed light on the broader question of lissamphibian origins and relationships has not been as thoroughly explored. Herein we review the morphology of the inner ear of the least well-known lissamphibian group, the caecilians, and present three-dimensional reconstructions of otic capsule endocasts and of soft-tissue labyrinths. We use these data to explore previous statements about the structure of the caecilian inner ear and its evolutionary significance. The postulate that the periotic canal has a posterior path is corroborated, and the periotic sacs of each ear are observed to extend into the brain cavity, where they are applied to a fluid-filled compartment that is located ventral to the brain. These features are shared with frogs and salamanders. Additionally, it is hypothesized that the regression of two endorgans in caecilians is correlated with the secondary loss of the two middle ear auditory pathways, the tympanum-stapes and opercularis hearing pathway, suggesting that the lissamphibian-type ear is present, but in a derived state in caecilians. Identification of osteological correlates of this lissamphibian-type ear permits the interpretation of the evolution of this distinct ear type in the context of the three competing hypotheses of lissamphibian phylogeny. The distribution of traits is shown to be most parsimoniously explained when optimized onto the phylogenetic pattern that incorporates a monophyletic temnospondyl-derived Lissamphibia. This interpretation is consistent with a single origin of a lissamphibian-type tympanic ear. Therefore, characters of the ear seemingly provide synapomorphies that unite lissamphibians with amphibamid temnospondyls, potentially improving the resolution of concepts about the affinities of frogs, salamanders, and caecilians and clarifying issues of tetrapod ear evolution.

Cranial Morphology of the Carboniferous-Permian Tetrapod Brachydectes newberryi (Lepospondyli, Lysorophia): New Data from µCT

“…Similar morphology of the otic region has recently been described in the microsaur Dvellecanus carrolli [42], as well as various amniotes [72, 75]. Importantly, the crista interfenestralis precludes a posterior course of the perilymph circulation, seen in all lissamphibians [1] and some temnospondyls [88], and thus suggests an anterior path of the perilymph circulation, as in amniotes.…”

The Braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the Origin of Caecilians

“…An additional element resembling a small disc-like bone, closely associated with the fenestra vestibuli and stapes-quadrate, was interpreted as an operculum [14]. An alternative hypothesis is one in which the element identified as the operculum is the stapes, and the larger element consists of the quadrate alone [14], [16].…”

“…The matrix of Anderson et al [18] was modified as per Maddin and Anderson [16], with additional amendments made here (see Table S1 in supporting information ). Modifications to the matrix of Maddin et al [28] include revised definitions of several characters that make them relevant to non-caecilian taxa, as well as 28 character exclusions due to redundancy with characters in Anderson et al [18] or autapomorphy.…”

“…Only a few phylogenetic analyses that include E. micropodia also include extant caecilians [16], [17], but more often E. micropodia is included to represent gymnophionans (e.g., [18]), thus precluding such an evaluation. Additionally, Gower and Wilkinson [5] have questioned, on the basis of several features, the validity of E. micropodia as representative of the plesiomorphic condition of caecilians, and Müller [19] raised the possibility that E. micropodia may actually occupy an alternative position within dissorophoid temnospondyl phylogeny.…”

Triadobatrachus massinoti, the earliest known lissamphibian (Vertebrata: Tetrapoda) re-examined by μCT scan, and the evolution of trunk length in batrachians

“…Under the phylogenetic hypotheses on the origin of lissamphibians currently defended in the literature, lissamphibians are closest relatives to either amphibamid temnospondyls (Ruta and Coates, 2007;Maddin and Anderson, 2012) or lysorophian lepospondyls (Vallin and Laurin, 2004;Marjanović and Laurin, 2013). In both cases, the most recent possible sister taxa date back to the Cisuralian (Early Permian, 299 -271 Ma), leaving a temporal gap of at least ~20 My between them and Triadobatrachus.…”