Endocranial anatomy of the early prozostrodonts (Eucynodontia: Probainognathia) and the neurosensory evolution in mammal forerunners

Abstract

Prozostrodon brasiliensis and Therioherpeton cargnini are non‐mammaliaform cynodonts that lived ~233 million years ago (late Carnian, Late Triassic) in western Gondwana. They represent some of the earliest divergent members of the clade Prozostrodontia, which includes “tritheledontids”, tritylodontids, “brasilodontids”, and mammaliaforms (including Mammalia as crown group). Here, we studied the endocranial anatomy (cranial endocast, nerves, vessels, ducts, ear region, and nasal cavity) of these two species. Our findings suggest that during the Carnian, early prozostrodonts had a brain with well‐developed olfactory bulbs, expanded cerebral hemispheres divided by the interhemispheric sulcus, and absence of an unossified zone and pineal body. The morphology of the maxillary canal represents the necessary condition for the presence of facial vibrissae. A slight decrease in encephalization is observed at the origin of the clade Prozostrodontia. This new anatomical information provides evidence for the evolution of endocranial traits of the first prozotrodonts, a Late Triassic lineage that culminated in the origin of mammals.

The origin and evolution of Cynodontia (Synapsida, Therapsida): Reassessment of the phylogeny and systematics of the earliest members of this clade using 3D‐imaging technologies

“…However, although strong variability characterizes the morphology of these endocranial characters, certain features appear generally static among non-probainognathian cynodonts, such as that the maxillary canal retains all its ramifications, a connection of the zygomaticofacial canal with the lacrimal canal, and the presence of a cochlear recess of the bony labyrinth in most of the investigated cynodont taxa. By contrast, an anteroposteriorly extensive maxillary sinus appears to be restricted to cynognathians (or at least gomphodonts) (see Figure 9o,p; also Benoit et al, 2018;Crompton et al, 2015), with the sinus in non-eucynodonts and probainognathians being much smaller (Figure 9c-n; Benoit A lateral position of the fenestra ovalis on the vestibule seems to be a common condition in all cynodonts with subtriangular vestibules (e.g., Kerber et al, 2024;Kielan-Jaworowska et al, 2004;Luo, 2001;Pusch et al, 2019Pusch et al, , 2023, but in Boreogomphodon, the fenestra vestibuli is positioned at the distal end of the vestibule. This is generally considered the primitive condition, observed widely in non-cynodont therapsids (e.g., Araújo et al, 2018;Bendel et al, 2018;Benoit et al, 2021;Castanhinha et al, 2013;Laaß, 2016;Pusch et al, 2020), but is here the result of the inflated shape of the vestibule, a rare condition in non-mammalian therapsids, which has previously only been described for the anomodont Kawingasaurus fossilis (Laaß, 2015a).…”

“…Discrete characters of the bony labyrinth (146): "Semicircular canal length: anterior longest (0), lateral longest (1), posterior longest (2)." In all but two of the sampled taxa for which bony labyrinths could be reconstructed, that is, Olivierosuchus, Theriognathus, Abdalodon muchingaensis, Procynosuchus, Cynosaurus, Vetusodon, Progalesaurus, Galesaurus, Thrinaxodon, Nanictosaurus, Platycraniellus, Trirachodon kannemeyeri, Boreogomphodon, and Lumkuia, the anterior semicircular canal is the longest of the three semicircular canals (Figure 11b-i,k-r) (see also Supporting Information Data 5: Tables S10 and S11), as in most other therapsids (e.g., Araújo et al, 2017Araújo et al, , 2018Bendel et al, 2018;Benoit et al, 2021;Castanhinha et al, 2013;Kerber et al, 2024;Kielan-Jaworowska et al, 2004;Laaß, 2016;Luo, 2001;Olson, 1944;Pusch et al, 2019;Rodrigues et al, 2013). By contrast, in the basal therocephalian Lycosuchus, the lateral semicircular canal appears to be the longest of the three semicircular canals (Figure 11a; Pusch et al, 2020), whereas in the early cynodont Nythosaurus, the posterior semicircular canal is longest of the three semicircular canals (Figure 11j; Pusch et al, 2023) (see also Supporting Information Data 5: Tables S10 and S11).…”

“…This technology has been instrumental in understanding such topics as tooth replacement, internal snout and braincase morphology, brain and bony labyrinth evolution, facial innervation, and the origins of endothermy in synapsids. Although endocranial characters have been described for various therapsids in CT-assisted studies in recent years (e.g., Araújo et al, 2017Araújo et al, , 2018Bendel et al, 2018;Benoit et al, 2018Benoit et al, , 2019Benoit et al, , 2021Benoit et al, , 2022Benoit, Jasinoski, Fernandez, & Abdala, 2017;Benoit, Manger, Fernandez, & Rubidge, 2016, 2017Castanhinha et al, 2013;Duhamel et al, 2021;Gigliotti et al, 2023;Laaß, 2015aLaaß, , 2015bLaaß, , 2016Pusch et al, 2020), with special focus on cynodonts due to their importance for mammal origins (e.g., Abdala et al, 2013;Benoit, 2023;Crompton, 2013;Crompton et al, 2015;Crompton, Owerkowicz, et al, 2017;Huttenlocker & Sidor, 2020;Jasinoski et al, 2015;Kemp, 2009;Kerber et al, 2021Kerber et al, , 2024Norton et al, 2020Norton et al, , 2021Pavanatto et al, 2019;Pusch et al, 2019Pusch et al, , 2021Pusch et al, , 2023Rodrigues et al, 2013Rodrigues et al, , 2014Rodrigues et al, , 2018Rowe et al, 1995…”

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

“…Nevertheless, it has been widely accepted that the nasal cavity of nonmammalian synapsids contained a system of cartilaginous turbinates. This view is supported by the presence of bony ridges on the inner walls of the nasal cavity, which were interpreted as sites for the attachment of the turbinates (e.g., Bendel et al, 2018;Crompton et al, 2015Crompton et al, , 2017Franco et al, 2021;Hillenius, 1992Hillenius, , 1994Kemp, 1979;Kerber et al, 2020Kerber et al, , 2023Pusch et al, 2019Pusch et al, , 2020Ruben et al, 2012). The pioneer work on the anatomy of the mammalian nasal skeleton was by Zuckerkandl (1887) and Paulli (1900aPaulli ( , 1900bPaulli ( , 1900c.…”

“…Nasoturbinal ridges (ntr) were already recognized on the undersides of the nasals and frontals in the nasal cavity of the sphenacodontid pelycosaur Dimetrodon (Romer & Price, 1940), as well as in numerous nonmammalian therapsids (e.g., Bendel et al, 2018;Brink, 1960;Cluver, 1971;Crompton et al, 2015Crompton et al, , 2017Fourie, 1974;Maier et al, 1996;Hillenius, 1994;Kemp, 1969Kemp, , 1979Kerber et al, 2020Kerber et al, , 2023Pusch et al, 2019Pusch et al, , 2020Ruf et al, 2014;Sigurdsen, 2006;Sigurdsen et al, 2012). Furthermore, several studies, which were based on X-ray computed tomography, focused on the nasal anatomy of modern mammals (e.g., Crompton et al, 2017;Macrini, 2012;Rowe et al, 2005;Ruf, 2020;Ruf et al, 2021;Van Valkenburgh et al, 2004).…”