Influence of fossoriality on inner ear morphology: insights from caecilian amphibians

Abstract

It is widely accepted that a relationship exists between inner ear morphology and functional aspects of an animal's biology, such as locomotor behaviour. Animals that engage in agile and spatially complex behaviours possess semicircular canals that morphologically maximise sensitivity to correspondingly complex physical stimuli. Stemming from the prediction that fossorial tetrapods require a well-developed sense of spatial awareness, we investigate the hypothesis that fossoriality leads to inner ear morphology that is convergent with other spatially adept tetrapods. We apply morphometrics to otic capsule endocasts of 26 caecilian species to quantify aspects of inner ear shape, and compare these with a sample of frog and salamander species. Our results reveal caecilians (and also frogs) possess strongly curved canals, a feature in common with spatially adept species. However, significantly shorter canals in caecilians suggest reduced sensitivity, possibly associated with reduced reliance on vestibulo-ocular reflexes in this group of visually degenerate tetrapods. An elaboration of the sacculus of caecilians is interpreted as a unique adaptation among amphibians to increase sensitivity to substrate-borne vibrations transmitted through the head. This study represents the first quantitative analyses of inner ear morphology of limbless fossorial tetrapods, and identifies features within a new behavioural context that will contribute to our understanding of the biological consequences of physical stimuli on sensory function and associated morphological evolution.

Bony labyrinth morphometry indicates locomotor adaptations in the squirrel-related clade (Rodentia, Mammalia)

“…However, with the benefits of modern non-invasive imaging techniques, such as high-resolution computed tomography (mCT), the first aspect has become a favourite topic for functional morphological analyses (e.g. [2][3][4][5][6][7][8][9][10][11][12][13]), but also for phylogenetic approaches [14 -20].…”

Bony labyrinth morphometry reveals hidden diversity in lungless salamanders (Family Plethodontidae): Structural correlates of ecology, development, and vision in the inner ear

“…Trends toward reduced curvature of the semicircular canals are also observed in fossorial caecilians with reduced visual systems (Maddin and Sherratt 2014). Trends toward reduced curvature of the semicircular canals are also observed in fossorial caecilians with reduced visual systems (Maddin and Sherratt 2014).…”

“…Because several histological specimens presented incomplete data for whole head measurements such as skull length, we calculated head size using a proxy measurement of the distance separating the two otic endocasts at the medial margin of the pars superior and pars inferior, following Maddin and Sherratt (2014). Additionally, we measured the total volume of the stapes, and the medial surface area of the stapes footplate.…”

“…Sensory traits integrate ontogeny (e.g., metamorphic changes to the amphibian visual [Hoskins 1990], mechanosensory lateral line [Fritzsch 1988;Roth et al 1992], and olfactory [Reiss and Eisthen 2008] systems), physiological demands, and ecological pressures experienced by organisms; therefore, variability of sensory structures among closely related species may reveal ecological specialization. For example, fossorial (burrowing) mammals (Burda et al 1992;Mason 2004), lizards (Toerien 1963), snakes (Yi and Norell 2015), and amphibians (Maddin and Sherratt 2014) exhibit repeated, parallel evolution of hypertrophic auditory structures believed to contribute to enhanced seismic sensitivity to ground vibrations. Although the inner ear is a functionally constrained structure (i.e., its features are phylogenetically conservative and gross morphological similarities exist at high organizational levels), structural variation of the components of the ear correlates with functional differences and sensory specializations among ecologically diverse species.…”

“…Further, structures related to sensory perception of environmental stimuli demonstrate a strong form-function relationship and thus are useful for investigating ecomorphological variation (Bock and von Wahlert 1965). Additionally, the size and shape of the semicircular canals are correlated with locomotor behavior in a broad range of vertebrate taxa that perform agile and/or spatially complex behaviors, including arboreal Anolis lizard ecomorphs (Dickson et al 2017), fossorial caecilian amphibians (Maddin and Sherratt 2014), gliding snakes (Boistel et al 2011), andfossorial, aquatic, andarboreal mammals (Lindenlaub et al 1995;Spoor et al 2002;Spoor 2003;Pfaff et al 2015). For example, fossorial (burrowing) mammals (Burda et al 1992;Mason 2004), lizards (Toerien 1963), snakes (Yi and Norell 2015), and amphibians (Maddin and Sherratt 2014) exhibit repeated, parallel evolution of hypertrophic auditory structures believed to contribute to enhanced seismic sensitivity to ground vibrations.…”