Fissures, folds, and scrolls: The ontogenetic basis for complexity of the nasal cavity in a fruit bat (Rousettus leschenaultii)

Abstract

Mammalian nasal capsule development has been described in only a few cross‐sectional age series, rendering it difficult to infer developmental mechanisms that influence adult morphology. Here we examined a sample of Leschenault's rousette fruit bats (Rousettus leschenaultii) ranging in age from embryonic to adult (n = 13). We examined serially sectioned coronal histological specimens and used micro‐computed tomography scans to visualize morphology in two older specimens. We found that the development of the nasal capsule in Rousettus proceeds similarly to many previously described mammals, following a general theme in which the central (i.e., septal) region matures into capsular cartilage before peripheral regions, and rostral parts of the septum and paries nasi mature before caudal parts. The ossification of turbinals also generally follows a rostral to the caudal pattern. Our results suggest discrete mechanisms for increasing complexity of the nasal capsule, some of which are restricted to the late embryonic and early fetal timeframe, including fissuration and mesenchymal proliferation. During fetal and early postnatal ontogeny, appositional and interstitial chondral growth of cartilage modifies the capsular template. Postnatally, appositional bone growth and pneumatization render greater complexity to individual structures and spaces. Future studies that focus on the relative contribution of each mechanism during development may draw critical inferences how nasal morphology is reflective of, or deviates from the original fetal template. A comparison of other chiropterans to nasal development in Rousettus could reveal phylogenetic patterns (whether ancestral or derived) or the developmental basis for specializations relating to respiration, olfaction, or laryngeal echolocation.

The dog–human connection

“…They note the capacity of turbinals to embark on secondary dermal bony expansion may be especially affected. This supports other recent studies that find turbinal complexity increases postnatally during snout growth (Smith, Curtis, Bhatnagar, & Santana, 2020; Smith, Martell, Rossie, Bonar, & DeLeon, 2016), perhaps as an epigenetic phenomena relating to respiratory physiology (Coppola, Craven, Seeger, & Weiler, 2014).…”

On the Embryonic Development of the Nasal Turbinals and Their Homology in Bats

“…Prenatally, the nasal epithelium sinks at specific sites, where the initial folds are created. Within the initial folds, mesenchymal condensations constitute the primitive morphology of the chondral template of turbinals (Smith et al, 2020). Later, these mesenchymal condensations chondrify.…”

“…Later, these mesenchymal condensations chondrify. In perinatal and postnatal stages, cartilages change their shape into lamellae (Smith et al, 2020). In the adult, the cartilaginous lamellae is fully ossified with the process of endochondral ossification except for the marginoturbinal and atrioturbinal (Voit, 1909;Martineau-Doizé et al, 1992;Ruf et al, 2015;Smith et al, 2020).…”

“…In perinatal and postnatal stages, cartilages change their shape into lamellae (Smith et al, 2020). In the adult, the cartilaginous lamellae is fully ossified with the process of endochondral ossification except for the marginoturbinal and atrioturbinal (Voit, 1909;Martineau-Doizé et al, 1992;Ruf et al, 2015;Smith et al, 2020). Additional turbinals branch off from each turbinal, scroll, and fold and also merge with one another (Parker, 1885;Maier, 1980Maier, , 2000Deleon and Smith, 2014;Maier and Ruf, 2014;Smith et al, 2020).…”

Inward collapse of the nasal cavity: Perinatal consolidation of the midface and cranial base in primates

“…Video can be viewed at https:// studio.brightcove.com/products/videocloud/media/videos/6200578659001 described at that age (Maier, 2000;Smith et al, 2017;Zeller, 1987). While some other regions of the chondrocranium are also observed to have delayed ossification (e.g., parts of the temporal bone), all midline elements posterior to the nasal capsule begin ossification prior to birth, while leaving synchondroses for continued interstitial expansion (Smith, Curtis, Bhatnagar, & Santana, 2020;Starck, 1967).…”