The nasal capsule, as the most rostral part of the chondrocranium, is a critical point of connection with the facial skeleton. Its fate may influence facial form, and the varied fates of cartilage may be a vehicle contributing to morphological diversity. Here, we review ontogenetic changes in the cartilaginous nasal capsule of mammals, and make new observations on perinatal specimens of two chiropteran species of different suborders. Our observations reveal some commonalities between
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 (
- NSF-PAR ID:
- 10452651
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- The Anatomical Record
- Volume:
- 304
- Issue:
- 4
- ISSN:
- 1932-8486
- Page Range / eLocation ID:
- p. 883-900
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Rousettus leschenaultii andDesmodus rotundus , such as perinatal ossification of the first ethmoturbinal. However, inRousettus , ossification of turbinals is demonstrated as either perichondrial or endochondral. InDesmodus , perichondrial and endochondral ossification of the posterior nasal cupula is observed at birth, a part of the nasal capsule previously shown to persist as cartilage into infancy inRousettus . Combined with prior findings on cranial cartilages we identify several diverse transformational mechanisms by which cartilage as a tissue type may contribute to morphological diversity of the cranium. First, cartilage differentiates in an iterative fashion to increase nasal complexity, but still retains the capacity for later elaboration via de novo bone emanating outward before or after cartilage ossifies. Second, cartilage acts as a driver of growth at growth centers, or via interstitial growth (e.g., septal cartilage). Finally, cartilage as a tissue may influence the timing of ossification and union of the facial and basicranial skeleton. In particular, cartilage at certain points of ontogeny may “model” via selective resorption, showing some similarity to bone. -
more » « less
Abstract Living primates show a complex trend in reduction of nasal cavity spaces and structures due to moderate to severe constraint on interorbital breadth. Here we describe the ontogeny of the posterior end of the primate cartilaginous nasal capsule, the thimble shaped posterior nasal cupula (PNC), which surrounds the hind end of the olfactory region. We used a histologically sectioned sample of strepsirrhine primates and two non‐primates (
Tupaia belangeri ,Rousettus leschenaulti ), and histochemical and immunohistochemical methods to study the PNC in a perinatal sample. At birth, most strepsirrhines possess only fragments of PNC, and these lack a perichondrium. Fetal specimens of several species reveal a more complete PNC, but the cartilage exhibits uneven or weak reactivity to type II collagen antibodies. Moreover, there is relatively less matrix than in the septal cartilage, resulting in clustering of chondrocytes, some of which are in direct contact with adjacent connective tissues. In one primate (Varecia spp.) and both non‐primates, the PNC has a perichondrium at birth. In older, infantVarecia andRousettus , the perichondrium of the PNC is absent, and PNC fragmentation at its posterior pole has occurred in the former. Loss of the perichondrium for the PNC appears to precede resorption of the posterior end of the nasal capsule. These results suggest that the consolidation of the basicranial and facial skeletons happens ontogenetically earlier in primates than other mammals. We hypothesize that early loss of cartilage at the sphenoethmoidal articulation limits chondral mechanisms for nasal complexity, such as interstitial expansion or endochondral ossification. -
Nasal turbinals, scrolled thin bones of the nasal cavity, increase surface area for conditioning inspired air or for olfaction in mammals. To assess function in Eptesicus fuscus (Big Brown Bat), we quantify surface area of respiratory and olfactory turbinals from birth to adult size, using data from microCT scans before and after iodine staining. Surface area of each turbinal is significantly correlated with postnatal age and cranial length. The surface area of the maxilloturbinal and first ethmoturbinal (ET I) grows faster, relative to skull size, than surface area of caudal ethmoturbinals or the frontoturbinal. Histological examination of selected specimens reveals ET I grows disproportionately more presumptive respiratory mucosa than olfactory mucosa, supporting the hypothesis that ET I has a dual function. Lastly, we find that distribution of olfactory mucosa in the caudal nasal cavity diminishes with age. Our findings suggest a reduction in olfactory function in E. fuscus, perhaps due to a diminished role in food acquisition by this aerial insectivore.more » « less
-
more » « less
Abstract The evolution of avian cranial kinesis is a phenomenon in part responsible for the remarkable diversity of avian feeding adaptations observable today. Although osteological, developmental and behavioral features of the feeding system are frequently studied, comparatively little is known about cranial joint skeletal tissue composition and morphology from a microscopic perspective. These data are key to understanding the developmental, biomechanical and evolutionary underpinnings of kinesis. Therefore, here we investigated joint microstructure in juvenile and adult mallard ducks (
Anas platyrhynchos ; Anseriformes). Ducks belong to a diverse clade of galloanseriform birds, have derived adaptations for herbivory and kinesis, and are model organisms in developmental biology. Thus, new insights into their cranial functional morphology will refine our understanding of avian cranial evolution. A total of five specimens (two ducklings and three adults) were histologically sampled, and two additional specimens (a duckling and an adult) were subjected to micro‐computed tomographic scanning. Five intracranial joints were sampled: the jaw joint (quadrate‐articular); otic joint (quadrate‐squamosal); palatobasal joint (parasphenoid‐pterygoid); the mandibular symphysis (dentary‐dentary); and the craniofacial hinge (a complex flexion zone involving four different pairs of skeletal elements). In both the ducklings and adults, the jaw, otic and palatobasal joints are all synovial, with a synovial cavity and articular cartilage on each surface (i.e. bichondral joints) ensheathed in a fibrous capsule. The craniofacial hinge begins as an ensemble of patent sutures in the duckling, but in the adult it becomes more complex: laterally it is synovial; whereas medially, it is synostosed by a bridge of chondroid bone. We hypothesize that it is chondroid bone that provides some of the flexible properties of this joint. The heavily innervated mandibular symphysis is already fused in the ducklings and remains as such in the adult. The results of this study will serve as reference for documenting avian cranial kinesis from a microanatomical perspective. The formation of: (i) secondary articular cartilage on the membrane bones of extant birds; and (ii) their unique ability to form movable synovial joints within two or more membrane bones (i.e. within their dermatocranium) might have played a role in the origin and evolution of modern avian cranial kinesis during dinosaur evolution. -
more » « less
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 andRhinella 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.
