Evolutionary Patterns of Trait Change in the Auditory System of Central American Toads (Anura: Bufonidae: Incilius)
The tympanic middle ear (TME) is a complex morphological adaptation that facilitates auditory reception in multiple clades of tetrapods, including anurans. Despite its utility, it has been partially or completely lost at least 38 times in anurans, and there is no clear explanation for how or why this loss occurred. We used micro-CT scans and 3D segmentation to catalog presence/absence and shape of the columella throughout the Central American toad genus Incilius. We found that the TME has been lost multiple times in Incilius and our outgroup Rhinella, with at least one regaining event. Absence of the columella and the different shapes of the columella both have high phylogenetic signal. Incilius species have a different distribution of columella shapes than many other genera of anurans that have been surveyed, including more blade-shaped columellae than found in other genera and one species with vestigial remnants of a columella. The columella shape most common in Incilius, a blade, may be derived from the rod shape also found in many other bufonids; the adaptive significance of this trait remains unknown. This study succeeds in providing a fine-scale review of earlessness and columellar morphology in Incilius, but the processes underlying the patterns we observe remain unclear.ABSTRACT
(A) Articulated skull of Incilius luetkenii, with columella shown in red. (B) Dorsal view of I. luetkenii columella (blade). (C) Posterior view of I. luetkenii columella (blade). (D) Lateral view of I. luetkenii columella (blade). (E) Articulated skull of I. coniferus, with columella shown in red. (F) Dorsal view of I. coniferus columella (rod). (G) Posterior view of I. coniferus columella (rod). (H) Lateral view of I. coniferus columella (rod). (I) Articulated skull of I. tacanensis, with columella shown in red. (J) Dorsal view of I. tacanensis columella (vestigial). (K) Posterior view of I. tacanensis columella (vestigial). (L) Lateral view of I. tacanensis columella (vestigial).
Phylogenetic tree of Incilius and outgroups (from Schachat et al., 2016), with character states of the columella (present is dark blue, absent is teal) and tympanum (present is green, absent is light blue) along the tips.
State change diagrams showing different rates of state change between a rod-shaped columella, blade-shaped columella, and absent columella and AICc scores for different models of character evolution, with the best-fitting model (the ER model) depicted in bold.
(A) Consensus tree of 1000 stochastic character maps of the ancestral presence/absence of the columella in Incilius generated under an ER model. Percent likelihood of columella presence/absence at each node is displayed as a pie chart; yellow indicates columella presence, and blue indicates columella absence. (B) Consensus tree of 1000 stochastic character maps of the ancestral shape of the columella in Incilius generated under an ER model. Percent likelihood of an absent/blade-shaped/rod-shaped columella at each node is displayed as a pie chart; blue indicates columella absence, red indicates a blade-shaped columella, and green indicates a rod-shaped columella.
Photograph of dissected specimen of I. occidentalis (UTA-A56321; adult male, SVL = 58.8 mm) showing the tympanic membrane, which is not externally visible in this species or in I. mccoyi (UTA-A61311, not shown).
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