Whispers from vestigial nubbins: Arrested development provokes trait loss in toads

Abstract

Despite the use of acoustic communication, many species of toads (family Bufonidae) have lost parts of the tympanic middle ear, representing at least 12 independent evolutionary occurrences of trait loss. The comparative development of the tympanic middle ear in toads is poorly understood. Here, we compared middle ear development among two pairs of closely related toad species in the genera Atelopus and Rhinella that have (eared) or lack (earless) middle ear structures. We bred toads in Peru and Ecuador, preserved developmental series from tadpoles to juveniles, and examined ontogenetic timing and volume of the otic capsule, oval window, operculum, opercularis muscle, columella (stapes), and extracolumella in three‐dimensional histological reconstructions. All species had similar ontogenesis of the otic capsule, oval window, operculum, and opercularis muscle. Moreover, cell clusters of primordial columella in the oval window appeared just before metamorphosis in both eared and earless lineages. However, in earless lineages, the cell clusters either remained as small nubbins or cell buds in the location of the columella footplate within the oval window or disappeared by juvenile and adult stages. Thus, columella growth began around metamorphosis in all species but was truncated and/or degenerated after metamorphosis in earless species, leaving earless adults with morphology typical of metamorphic anurans. Shifts in the timing or expression of biochemical pathways that regulate the extension or differentiation of the columella after metamorphosis may be the developmental mechanism underlying convergent trait loss among toad lineages.

Convergent Anuran Middle Ear Loss Lacks a Universal, Adaptive Explanation

“…Neither study found consistent phenotypic differences between eared and earless species. Other studies have investigated whether tympanic middle ear loss is a side effect of changes in developmental timing or rate (heterochrony), but none have found consistent shifts in development among earless species [77,[82][83][84]. However, these studies did not exhaustively quantify earless species phenotypes, making it possible that a shared developmental or phenotypic change exists among earless taxa.…”

“…However, these studies did not exhaustively quantify earless species phenotypes, making it possible that a shared developmental or phenotypic change exists among earless taxa. Given the nearly unlimited potential pleiotropic connections between the tympanic middle ear and other traits, genetic scans for mutations associated with tympanic middle ear loss and comparative developmental studies that examine changes during the window of arrested tympanic middle ear development [77] would allow a more thorough examination of this hypothesis.…”

“…It is possible tympanic middle ears carry a common cost that has not been measured yet. However, earless frogs incur the energetic costs of maintaining hearing pathways and neural cir-cuitry, as low frequency hearing via bone conduction and other nontympanic hearing pathways are preserved, and earless frogs do not noticeably differ in their inner ear structures [54,77]. Additionally, although a number of organisms, such as parasitic trematodes, are known to parasitize the tympanic middle ear cavity and can affect hearing [78,79], the overlapping ranges of eared and earless species do not provide confidence that increased parasite risk promotes tympanic middle ear loss.…”

Unraveling the heritage of lost traits

“…Numerous anuran clades have vestigial middle structures, in which some earlier developing structures of the middle ear remain (Pereyra et al, 2016) but seemingly lack any hearing‐related function (Womack et al, 2018). Other middle ear loss clades have transient middle ear structures during development but completely lack middle ear structures as adults (Stynoski et al, 2020). Even within a population, some individuals show no trace of the middle ear as adults and others have small cartilaginous chunks of middle ear bone as adults (Stynoski et al, 2020).…”

“…Other middle ear loss clades have transient middle ear structures during development but completely lack middle ear structures as adults (Stynoski et al, 2020). Even within a population, some individuals show no trace of the middle ear as adults and others have small cartilaginous chunks of middle ear bone as adults (Stynoski et al, 2020). Similarly, forelimbs, hind limbs, and pelvic bones have been convergently lost to varying degrees among skink species with additional intraspecific variation in the degree of loss noted in some lineages (Moch & Senter, 2011).…”