Nasal turbinates of the dicynodont Kawingasaurus fossilis and the possible impact of the fossorial habitat on the evolution of endothermy

Abstract

The nasal region of the fossorial anomodont Kawingasaurus fossilis was virtually reconstructed from neutron‐computed tomographic data and compared with the terrestrial species Pristerodon mackayi and other nonmammalian synapsids. The tomography of the Kawingasaurus skull reveals a pattern of maxillo‐, naso‐, fronto‐ and ethmoturbinal ridges that strongly resemble the mammalian condition. On both sides of the nasal cavity, remains of scrolled maxilloturbinals were preserved that were still partially articulated with maxilloturbinal ridges. Furthermore, possible remains of the lamina semicircularis as well as fronto‐ or ethmoturbinals were found. In Kawingasaurus, the maxilloturbinal ridges were longer and stronger than in Pristerodon. Except for the nasoturbinal ridges, no other ridges in the olfactory region and no remains of turbinates were recognized. This supports the hypothesis that naso‐, fronto‐, ethmo‐ and maxilloturbinals were a plesiomorphic feature of synapsids, but due to their cartilaginous nature in most taxa were, in almost all cases, not preserved. The well‐developed maxilloturbinals in Kawingasaurus were probably an adaptation to hypoxia‐induced hyperventilation in the fossorial habitat, maintaining the high oxygen demands of Kawingasaurus' large brain. The surface area of the respiratory turbinates in Kawingasaurus falls into the mammalian range, which suggests that they functioned as a countercurrent exchange system for thermoregulation and conditioning of the respiratory airflow. Our results suggest that the environmental conditions of the fossorial habitat led to specific sensory adaptations, accompanied by a pulse in brain evolution and of endothermy in cistecephalids, ~50 million years before the origin of endothermy in the mammalian stem line. This supports the Nocturnal Bottleneck Theory, in that we found evidence for a similar evolutionary scenario in cistecephalids as proposed for early mammals.

New evidence from high-resolution computed microtomography of Triassic stem-mammal skulls from South America enhances discussions on turbinates before the origin of Mammaliaformes

“…All these structures are identified as for blood vessels or nerves 81 . Ruf et al 29 and Laaß and Kaestner 40 identified this groove as for the olfactory nerve; however, Angielczyk et al 85 interpreted it as the ophthalmic canals of the trigeminal nerve. Due to the grooves formed by the ethmoidal and lateral ridges are divided into branches anteriorly that end in the posterior border of the external nares would support the hypothesis that these grooves housed the olfactory nerve, as proposed by others 29 , 40 .…”

“…If turbinals were present in extinct groups of synapsids, such as “pelycosaurs”, therocephalians, non-mammaliaform cynodonts 19 , 27 – 39 , they remained cartilaginous 19 (but see 40 ); therefore, they are hardly preserved in the fossil record. Despite this, other structures can prove indirectly the presence of these cartilaginous tissues inside the nasal cavity of non-mammaliaform synapsids 19 , 28 , 29 , 31 , 33 .…”

“…Despite this, other structures can prove indirectly the presence of these cartilaginous tissues inside the nasal cavity of non-mammaliaform synapsids 19 , 28 , 29 , 31 , 33 . Recently, Laaß and Kaestner 40 described the presence of ossified maxilloturbinals for the fossorial anomodont dicynodont Kawingasaurus fossilis (late Permian of Tanzania). As a conclusion, the authors claimed the presence of endothermy in Permian cistecephalid dicynodonts 40 .…”

“…Recently, Laaß and Kaestner 40 described the presence of ossified maxilloturbinals for the fossorial anomodont dicynodont Kawingasaurus fossilis (late Permian of Tanzania). As a conclusion, the authors claimed the presence of endothermy in Permian cistecephalid dicynodonts 40 . In non-mammaliaform cynodonts (e.g., Bolotridon , Massetognathus , Probainognathus , Pseudotherium , Brasilodon ) ridges located in the lateral and dorsal surfaces of the nasal cavity were identified as attachment areas of the cartilaginous turbinals and nasal septum, respectively 29 , 31 , 33 , 38 , 39 .…”

“…The presence of the turbinals in extant mammals and of structures provisionally associated with the turbinals (the ridges on the wall of the nasal cavity) in non-mammaliaform synapsids is directly associated with an endothermic condition by some authors 8 , 19 , 29 , 31 , 34 , 38 , 40 . In this sense, we used here as definition of endothermy as the continuous generation of body heat through metabolic processes, maintaining a relatively constant internal temperature independently of external conditions (i.e., tachymetabolic endothermy sensu 41 ), excluding short-term torpor, aestivation, and hibernation phases 42 (for discussions on termoregulatory regimens and terminology in extant and extinct taxa, see also, for example, Griggs et al 41 , Clarke and Pörtner 43 , Lovegrove 44 , and Legendre and Davesne 45 ).…”