Ontogeny and phylogeny of the mammalian chondrocranium: the cupula nasi anterior and associated structures of the anterior head region

Abstract

Background: The study of chondrocrania has a long tradition with a focus on single specimens and stages. It revealed great interspecific diversity and a notion of intraspecific variation. As an embryonic structure, the chondrocranium is subject to major changes in ontogeny with resorption and ossification of different cartilaginous structures. The cupula nasi anterior is the anteriormost portion of the cartilaginous nasal capsule and is expected to mirror much of the animal's life history and lifestyle. Its diversity in mammals is reflected in the external nasal anatomy of newborns. Marsupials and placentals show marked differences, likely related to breathing and suckling behavior.

Results: We examined histological sections of five marsupial and three placentals species and traced the development of the cupula nasi anterior and the anterior nasal capsule. We found ontogenetic variation for nearly 50% of the 43 characters defined herein. By comparing to the literature and considering ontogenetic variation, we performed an analysis of character evolution in 70 mammalian species and reconstructed the nasal anatomy of the therian ancestor.

Conclusions: At birth, marsupials have a complete but simple cupula nasi anterior, whereas placentals display a more diverse morphology due to reductions and variations of chondrocranial elements. The more compact nasal capsule in marsupials is related to a long and strong fixation to the mother's teat after birth. Within marsupials and placentals, several derived characters distinguish major taxa, probably related to developmental and functional constraints. The reconstructed ancestral anatomy of the cupula nasi anterior supports the hypothesis that the therian ancestor was placental-like and that the marsupial lifestyle is more derived.

Keywords: Chondrocranium; Cupula nasi anterior; Mammalia; Ontogeny; Therian ancestor.

Fig. 1

General anatomy of the cartilaginous nose. a Scheme adopted from Maier [56] on the rostral nasal cartilage in an adult Neomys fodiens. Cartilage in blue, bones (only on right body side) in orange, soft tissue in gray. Cross-sections of a pouch young Caluromys philander; dpn (postnatal days) 30, HL (head length) 13 mm at the ethmoidal region with details of the cupula nasi anterior, b anterior wall of cartilago cupularis, c cartilago cupularis in the region of fenestra narina, d region posterior to the fenestra narina, e anterior margin of the zona annularis. Numbers of histological serial sections are indicated at the bottom right of each figure. Numbers ascend in caudal direction. Scale bars equal 1 mm. Abbreviations: ai – area internarica, ane – apertura nasi externa, at – atrioturbinale, cc – cartilago cupularis, cdn – cartilago ductus nasopalatini, cna – cupula nasi anterior, cpa – cartilago paraseptalis anterior, dnl – ductus nasolacrimalis, dnp – ductus nasopaltinus, fpt – foramen praetransversale, lat. lam – lateral lamina, lta – lamina transversalis anterior, mat – marginoturbinale, med. lam – medial lamina, pas – processus alaris superior, pc – processus cupularis, plv – processus lateralis ventralis, pmx – praemaxillare, pn – paries nasi, ppl – processus paralacrimalis, sn – septum nasi, ss – sulcus supraseptalis, sv – sulcus ventralis, tea – tectum nasi anterius, tei – tectum nasi intermedium, tep – tectum nasi profundum, tn – tectum nasi, vno – organon vomeronasale, vo – vomer, za – zona annularis

Fig. 2

Overview of the variable shape of the cupula nasi anterior in mammals. Lateral view on the left, dorsal on the right. Cartilage colorless, bones in grey. Characters and character states are indicated (e.g., 26–1). a Tachyglossus aculeatus, HL 27 mm [20], b Didelphis marsupialis, CRL 45.5 mm [42], c Wallabia rufogrisea, HL 12 mm [54], d Vombatus ursinus, HL 14 mm [52]. Drawings by Timea Bodogán, modified from cited sources. Not to scale. Continued in Fig. 4

Fig. 3

Cross sections of pouch young Monodelphis domestica where the ductus nasopalatinus opens to the nasal cavity, a CRL (crown-rump length) 11.5 mm, b CRL 63 mm. Transversal sections of the nasal capsule in (c) Petaurus breviceps, CRL 9 mm, and (d) Atelerix albiventris, dpc 25 (days post conception). Numbers of histological serial sections are indicated at the bottom right of each figure. Scale bars equal 500 μm. Continued in Fig. 5. Abbreviations: ai – area internarica, at – atrioturbinale, cc – cartilago cupularis, dnp – ductus nasopalatinus, fia – fenestra internasalis anterior, lat. Lam – lateral lamina, lta – lamina transversalis anterior, med. Lam – medial lamina, mt – maxilloturbinale, sn – septum nasi

Fig. 4

Overview of the variable shape of the cupula nasi anterior in mammals. Continued from Fig. 2. a Dasypus novemcinctus, CRL 40 mm [32], b Hemicentetes semispinosus, HL 14 mm [39], c Eremitalpa granti, CRL 28.5 mm [30], d Setifer setosus, CRL 20.4 mm [30]. Drawings by Timea Bodogán, modified from cited sources. Not to scale. Continued in Fig. 6

Fig. 5

Continued from Fig. 3. Cross sections of a pouch young Caluromys philander at the region of the opening of fenestra narina, a HL 6 mm, b HL 26 mm. Cross sections of a pouch young Macropus eugenii at the anterior region of the lamina transversalis anterior, c HL 11 mm, d HL 53 mm. Scale bars equal 500 μm

Fig. 6

Overview of the variable shape of the cupula nasi anterior in mammals. Continued from Fig. 4. a Orycteropus cuniculus, CRL 45 mm [8], b Octodontomys gliroides, HL 19 mm [22], c Phodopus sungorus, HL 11.5 mm [46]. Drawings by Timea Bodogán, modified from cited sources. Not to scale. Continued in Fig. 7

Fig. 7

Overview of the variable shape of the cupula nasi anterior in mammals. Continued from Fig. 6. a Ptilocercus lowii, CRL 45 mm [89], b Erinaceus europaeus, CRL 19 mm [6], c Cryptoprocta ferox, CRL 54 mm [15]. Drawings by Timea Bodogán, modified from cited sources. Not to scale

Fig. 8

Overview of the processes of the nasal capsule in Suncus orangiae, CRL 15.6 mm [30]. Lateral view on the left, ventral on the right. a Processus cupularis, processus alaris superior, and (b) sulcus ventralis. Drawings by Timea Bodogán, modified from cited source. Not to scale

Fig. 9

Ventral view of the cupula nasi anterior in ontogenetic series of marsupials. Characters and character states are indicated. Ontogenetic stages increase from left to right. a Monodelphis domestica: CRL 10.5 mm (ESUT-Mo10.5), 11.5 mm (ESUT-Mo11.5), 20.5 mm (ESUT-Mo8.5) and 63 mm (ESUT-Mo63), b Caluromys philander: HL 6 mm (ESUT-C6), 7.5 mm (ESUT-C15), 13 mm (ESUT-C13) and 26 mm (ESUT-C26), c Sminthopsis virginiae: HL 3.5 mm (AMNH SR 1A), 4.5 mm (AMNH SR 2A), 9 mm (AMNH SR 3A) and 11.5 mm (AMNH SR 4A), d Macropus eugenii: HL 11 mm (ESUT-M11), 16 mm (ESUT-M16), 28 mm (ESUT-M28) and 53 mm (ESUT-M53), e Petaurus breviceps: CRL 9 mm (LANE-P82A) and 11 mm (LANE-P48). Drawings from 3d-reconstructions. Not to scale

Fig. 10

Lateral view of the cupula nasi anterior in ontogenetic series of marsupials. Characters and character states are indicated. Ontogenetic stages increase from left to right. a Monodelphis domestica: CRL 10.5 mm (ESUT-Mo10.5), 11.5 mm (ESUT-Mo11.5), 20.5 mm (ESUT-Mo8.5) and 63 mm (ESUT-Mo63), b Caluromys philander: HL 6 mm (ESUT-C6), 7.5 mm (ESUT-C15), 13 mm (ESUT-C13) and 26 mm (ESUT-C26), c Sminthopsis virginiae: HL 3.5 mm (AMNH SR 1A), 4.5 mm (AMNH SR 2A), 9 mm (AMNH SR 3A) and 11.5 mm (AMNH SR 4A), d Macropus eugenii: HL 11 mm (ESUT-M11), 16 mm (ESUT-M16), 28 mm (ESUT-M28) and 53 mm (ESUT-M53), e Petaurus breviceps: CRL 9 mm (LANE-P82A) and 11 mm (LANE-P48). Drawings by Timea Bodogán from 3d-reconstructions. Not to scale

Fig. 11

Embryonic stages of placentals. a Echinops telfairi (LANE-Ech5a) (mirrored), b Echinops telfairi (LANE-Ech7a) (mirrored). c Acomys dimidiatus (LANE-Aco18, dpc 18), d Acomys dimidiatus (LANE-Aco21, dpc 21), d Atelerix albiventris (LANE-Atx21, dpc 21), d Atelerix albiventris (LANE-Atx25, dpc 25). Scale bars equal 1 mm, Echinops telfairi (A-B) not to scale

Fig. 12

Frontal view of adult placentals on the left, lateral view on the right. a Echinops telfairi, b Acomys dimidiatus, c Atelerix albiventris

Fig. 13

Phylogenetic framework and taxonomic sampling for the character mapping performed in this study. For details on phylogenetic arrangement, see text