Embryonic staging of bats with special reference to Vespertilio sinensis and its cochlear development

Abstract

Background How bats deviate heterochronically from other mammals remains largely unresolved, reflecting the lack of a quantitative staging framework allowing comparison among species. The standard event system (SES) is an embryonic staging system allowing quantitative detection of interspecific developmental variations. Here, the first SES‐based staging system for bats, using Asian parti‐colored bat (Vespertilio sinensis) is introduced. General aspects of normal embryonic development and the three‐dimensional development of the bat cochlea were described for the first time. Recoding the embryonic staging tables of 18 previously reported bat species and Mus musculus into the SES system, quantitative developmental comparisons were performed. Results It was found that limb bud development of V. sinensis is relatively late among 19 bat species and late limb development is a shared trait of vespertilionid bats. The inner ear cochlear canal forms before the semicircular canal in V. sinensis while the cochlear canal forms after the semicircular canal in non‐volant mammals. Conclusions The present approach using the SES system provides a powerful framework to detect the peculiarities of bat development. Incorporating the timing of gene expression patterns into the SES framework will further contribute to the understanding of the evolution of specialized features in bats.

Timing of organogenesis underscores the evolution of neonatal life histories and powered flight in bats

“…[29] and Nojiri et al . [33] to the dataset. We excluded some SES characters, which were not observed in mammals [49].…”

The vocal apparatus of bats: an understudied tool to reconstruct the evolutionary history of echolocation?

“…A similar protocol should be undertaken on bat larynges to provide a better illustration and knowledge of the potential morphotypes described in the literature. Studies focusing on other anatomical features of bats have been performed recently (Yohe et al 2018;Santana 2018;Santana et al 2019;Ito et al 2021;Nojiri et al 2021b;Sohn et al 2021) and some studies used CT and iodine contrastenhanced imaging techniques to answer hypotheses about the evolutionary history of bats, such as recent studies on the hearing apparatus (Nojiri et al 2021a, b;Sulser et al 2022). It will be highly valuable to illustrate the shape and size of the different cartilages, their degree of mineralisation, in addition to the size, shape and position of the different muscles involved in laryngeal echolocation, especially the cricothyroid and the thyrohyoid.…”

“…Therefore, the ontogeny of P. parnellii could potentially explain the evolutionary convergence of echolocation strategies with the Rhinolophids. In terms of anatomical research in the development of laryngeal echolocation, only a few research have been published regarding the relationship between anatomy and echolocation (e.g., Pedersen 1995;Nojiri et al 2021b). Some of that research considered the evolutionary aspect of laryngeal echolocation (e.g., Nojiri et al 2021a) and only the recent research in ontogeny focused on the laryngeal aspect of sound production and its implication in laryngeal echolocation development (e.g., Carter et al 2019;Carter 2020).…”

“…Some of that research considered the evolutionary aspect of laryngeal echolocation (e.g., Nojiri et al 2021a) and only the recent research in ontogeny focused on the laryngeal aspect of sound production and its implication in laryngeal echolocation development (e.g., Carter et al 2019;Carter 2020). These research highlighted that the ontogeny of the skull (Pedersen 1995) and of the cochlea (Carter and Adams 2016;Nojiri et al 2021b) illustrated some constraints by the demands of vocalisations in bats.…”

“…Further, they suggested that sensitivity and high-frequency production both appeared before the ability to fly and then the three capacities coevolved through time. The ontogeny of the cochlea has been described as accelerated compared to non-echolocator mammals (Nojiri et al 2021b) and among bats, specific developments of the hearing apparatus have illuminated several evolutionary pathways (Nojiri et al 2021a). The ontogeny of the hyoid apparatus and the intrinsic laryngeal cartilages shows correlations with the development of echolocation, and the different echolocation strategies have been implicated in the reinforcement by mineralisation/ossification of some parts of the cartilages during postnatal development (Carter et al 2019;Carter 2020).…”