Is there an exemplar taxon for modelling the evolution of early tetrapod hearing?

Christensen et al. recently published a study of hearing in neotenic and experimentally metamorphosed axolotls (Ambystoma mexicanum) and a larval and adult tiger salamander (A. tigrinum), which contributes greatly to our understanding of salamander sound perception in water and air [1]. They demonstrate that premetamorphic, atympanic aquatic salamanders are capable of perceiving high frequency airborne sounds similar to terrestrial adults, demonstrating an interesting capacity for an atympanic ear to function for sound perception in a variety of media. This important research, in combination with other recent studies on the sound perception capabilities of lungfish [2], is helping to better clarify issues related to the water-to-land transition. However, the implication of their experimental design demands a consideration of the evolutionary history of their selected exemplar taxa so these valuable data can be interpreted in a broader context. Our criticisms focus on two major points: the use of salamanders as a proxy for hearing ability intermediate between aquatic and terrestrial vertebrates, and the use of microsaurs as exemplars of the early tetrapod condition. The currently accepted hypothesis for the origin of a tympanic ear is as a derivation from the spiracle of sarcopterygian fish [3]. In ‘fish’ the spiracle is associated with gill breathing: water passes through the spiracular notch in the rear of the skull, past the braincase and the bracing hyomandibula, to the oropharynx and gill arches [4]. With the loss of gills, the persisting spiracular lumen is co-opted into a middle ear chamber, and the cranial support role of the hyomandibula (now termed stapes) is eliminated, leaving this bone to extend freely into the middle ear chamber (figure 1). In derived tetrapods, the spiracular opening is expanded and covered by a membrane (the tympanum) that collects sound. Vibrations are transmitted to the inner ear via the stapes, which becomes more delicate and better able to propagate fine vibrations [7–10].