Prenatal cranial bone development of Thomas's horseshoe bat (Rhinolophus thomasi): with special reference to petrosal morphology

Abstract

Cochlear morphology has been regarded as one of the key traits to understand the origin and evolution of echolocation in bats, given its functionality and performance for receiving echolocation sonar. While numerous researchers have compared adult-stage morphology, few have studied the prenatal development of the cochlea. Here, we provide the first detailed three-dimensional description of the prenatal cranial development in bats, using Rhinolophus thomasi as a model, with particular interest to the petrosal which houses the cochlea. Results revealed that among all cranial bones the onset of the ossification of the petrosal is earlier in R. thomasi when compared to other reported mammals. Generally, the cochlea reaches adult size and shape before or around birth in placental mammals including bats, but we found that its shape and size growths continue until maturity in Rhinolophus species. The relationship of cochlear size and skull size is maintained constant throughout the postnatal ontogeny to adulthood in Rhinolophus, a pattern previously reported neither in any other bats nor other mammals. The peculiar developmental pattern in Rhinolophus possibly allows them to form their characteristically large cochlea and facilitate their distinctive echolocation behavior. A recent study reported that non-echolocating Pteropodidae shares a similar prenatal cochlear size to laryngeal echolocating bats. The apparent resemblance of fetal cochlear size was proposed to be a vestigial signal of large cochlear size in the last common ancestor of bats and thus as supporting evidence for the single origin of laryngeal echolocation. However, results from the present observations suggest that limited aspects of the cochlear development were captured in this previous investigation and that the resulting interpretations may be questionable. We point out that diversity and patterns of cochlear development among bats are still not resolved, and the controversy on the origins of laryngeal echolocation is still open to discussion.

Prenatal allometric trajectories and the developmental basis of postcranial phenotypic diversity in bats (Chiroptera)

“…Similar results have been interpreted as evidence for an ontogenetic basis for shape disparity in the palate of phyllostomid bats, a family that exhibits the greatest cranial shape diversity within Chiroptera (Sears, ). Contrary to most studies that have focused on the evolution of the cranium where there was no ontogenetic signal in phylogenetic relationships (Nojiri et al, ; Wang et al, ), our results show a clear ontogenetic signal in the subordinal phylogenetic relationships in Chiroptera. Nevertheless, this does not exclude that other aspects of their biology could have played a significant role during their divergence.…”

“…Moreover, intraguild differences in postnatal growth have been reported between tropical and temperate insectivorous bat species (Kunz, Adams, & Wood, 2009 that have focused on the evolution of the cranium where there was no ontogenetic signal in phylogenetic relationships (Nojiri et al, 2018;Wang et al, 2017), our results show a clear ontogenetic signal in the subordinal phylogenetic relationships in Chiroptera. Nevertheless, this does not exclude that other aspects of their biology could have played a significant role during their divergence.…”

“…Yangochiroptera exhibited faster than average growth of the manual phalanges compared with Yinpterochiroptera (Koyabu & Son, ), suggesting a tendency towards precociality. However, considering the variability in the development between different regions of the body (i.e., altricial development of the autopod and precocial development of the foot compared with other mammals), bats are difficult to define as either precocial or altricial (Koyabu & Son, ; Nojiri et al, ). Slower growth of the thoracic, cervical, and lumbar vertebrae, on the other hand, indicates a shift in the prenatal ontogenesis of presacral vertebral development in the yinpterochiropterans examined here.…”

“…Based on this, it was argued that there was not a developmental signal in the subordinate partition of the order, and instead an autapomorphic change in the development of the cochlea in pteropodidae (Wang et al, ). However, this conclusion has also been challenged on the basis of developmental data (Nojiri et al, ), leaving the question of whether a developmental signal exists in the subordinal divergence in Chiroptera unresolved. Developmental studies in bats have also shown heterochronic acceleration in the development of the foot and thumb compared with other mammals (Koyabu & Son, ), the regulatory role that wing membrane has in the development of the wing (Adams, ), postnatal compensatory growth between the autopod and zeugopod (Adams, ; Adams & Shaw, ), and a developmental basis for the diversification of New World leaf‐nosed bats (Sears, ).…”

Three-Dimensional and Histological Observations on Male Genital Organs of Greater Horseshoe Bat, Rhinolophus ferrumequinum

“…The accessory genital glands, in particular, have been very difficult to observe using conventional techniques. Recently, microcomputed tomography (microCT) imaging has demonstrated tremendous potential in unraveling previously undescribed bat anatomy, mainly the penis and baculum (Herdina et al 2010(Herdina et al , 2015a, turbinal morphology(Curtis and Simmons 2017), vomeronasal and olfactory system (Yohe et al 2018), and prenatal cranial bone development (Nojiri et al 2018). Contrast enhancement methods (diceCT) by iodine staining, in particular, have opened up new avenues in the study of bony structures and soft tissues in detail using X-ray (Gignac and Kley 2014;Gignac et al 2016).…”