The Evolution of Tetrapod Ears and the Fossil Record

Abstract

In the earliest tetrapods, the fenestra vestibuli was a large hole in the braincase wall bounded by bones of different embryological origins: the otic capsule and occipital arch components, and also, in all except the Devonian Acanthostega, the dermal parasphenoid. This means that the hole lay along the line of the embryonic metotic fissure. Early tetrapod braincases were poorly ossified internally, and no specialized opening for a perilymphatic duct is evident. It is arguable that the earliest tetrapods had neither a perilymphatic duct crossing the otic capsule nor a specialized auditory receptor in a separate lagenar pouch. The primitive tetrapod condition is found in the earliest amniotes, and the separate development of (1) a fenestra vestibuli confined to the limits of the otic capsule, (2) a specialized pressure relief window also derived from components on the line of the metotic fissure, (3) a nonstructural, vibratory stapes and (4) increased internal ossification of the internal walls of the otic capsule, can be traced separately in synapsids, lepidosauromorph diapsids, archosauromorph diapsids, probably turtles, and amphibians. This suggests separate development of true tympanic ears in each of these groups. Developments indicating the existence of a true tympanic ear in amniotes are first found in animals from the Triassic period, and a correlation with the evolution of insect sound production is suggested.

Specialization for underwater hearing by the tympanic middle ear of the turtle,Trachemys scripta elegans

“…(d) Evolution of the turtle ear The tympanic ear originated independently in turtles [9]. Specializations for underwater hearing may reflect the primitive condition in turtles if they originated in aquatic habitats.…”

Population Coding of Interaural Time Differences in Gerbils and Barn Owls

“…Until recently, it was assumed that mammals also process ITDs in a manner similar to that proposed by Jeffress. However, tympanic ears (and, thus, ITD sensitivity) evolved separately in birds and mammals (Clack, 1997), and while there is some evidence for anatomical delay lines in the MSO (Smith et al, 1993;Beckius et al, 1999), they do not appear to account for the observed physiological delays (Karino et al, 2010). Furthermore, apart from an apparent weak gradient of preferred ITDs in the MSO (Yin and Chan, 1990;Oliver et al, 2003), most of the evidence suggests that there is no ITD-based space map in the ascending auditory pathway (Middlebrooks et al, 2002;Grothe, 2003;McAlpine and Grothe, 2003;King and Campbell, 2005;McAlpine, 2005;Joris and Yin, 2007).…”

Coding interaural time differences at low best frequencies in the barn owl

“…In the discussion we will identify similarities among the brainstem circuits that detect interaural time differences in birds and mammals, and argue that these are the result of parallel evolution (see review in [21]). Evidence for parallel evolution comes from the observation that tetrapod tympanic ears are not homologs, and may have evolved independently at least five times (modern representatives given in brackets) in synapsids (mammals), lepidosauromorph diapsids (snakes and lizards), archosauromorph diapsids (birds and crocodilians), probably turtles, and amphibians [23,69,70]. Wilcynzski [122] has argued that these peripheral changes would have different reorganizing effects upon the ancestral population of brainstem auditory neurons, leading to the parallel evolution of the central targets of the auditory nerve.…”