Functional implications of ear loss in sand lizards

Despite being a highly advantageous trait, tympanic hearing was secondarily lost multiple times within tetrapods. Typically, loss of a sensory structure implies a shift to new environments where selection for another trait inhibits the development of said sensory structure, or a relaxation of selection on the sensory organ. However, the loss of tympanic hearing within North American sand lizards (Phrynosomatidae: Callisaurini) has eluded explanation. To explore the evolutionary reduction and loss of tympanic hearing within this clade, we created 3D models of the stapes to analyze morphological differences. Then, we determined if those morphological differences impact stapedial movement using harmonic response analysis (HRA). We also included the stapes of the callisaurin sand lizards along with those of a diversity of other squamatans in a series of linear discriminant analyses to determine if stapes of tympanic and atympanic species differ morphologically, and if the presence or absence of limbs, lifestyle, or diet influence stapedial morphology. We found that both earless taxa (Cophosaurus, Holbrookia) possess stapes that are relatively short with a large footplate, similar to those of other atympanic squamatans, while the eared taxon Uma has a long and slender stapes, similar to those of other tympanic squamatans. However, the eared taxon Callisaurus possesses a stapes that is intermediate between those of Uma and the atympanic species. Similarly, it was less prone to displacement within the HRA than other eared species. We found that neither lifestyle nor diet could explain differences in ear morphology within this clade. This suggests that ear loss in this clade is either due to a relaxation of selection on the ear, or more likely, differences in substrate use when the lizards bury themselves resulted in selection on the ear that influences both stapedial shape and tympanum loss, perhaps for the transmission of low-frequency vibrations through substrate. The combination of a tympanum with a broad stapes in Callisaurus, in the context of the other sand lizard genera, suggests that modification to the stapes and quadrate may precede the formation or loss of a tympanum, which has implications for interpreting the evolutionary origins of hearing from fossils.