Digital cranial endocast of Riograndia guaibensis (Late Triassic,Brazil) sheds light on the evolution of the brain in non-mammalian cynodonts

Abstract

A digital cranial endocast of the specimen UFRGS-PV-596-T of Riograndia guaibensis was obtained from μCT scan images. This is a small cynodont, closely related to mammaliaforms, from the Late Triassic of Brazil. Riograndia has large olfactory bulb casts and the cerebral hemispheres region is relatively wider than in other non-mammaliaform cynodonts. Impressions of vessels were observed and a conspicuous mark on the dorsal surface was interpreted as the transverse sinus. The calculated encephalization quotient is greater than the range seen in most other non-mammaliaform cynodonts. The ratios between linear and area measurements of the dorsal surface suggest four evolutionary changes from a basal eucynodont morphology to mammaliaforms, involving an evolutionary increase of the relative size of the olfactory bulbs and the width of the cerebral hemispheres and cerebellum. The data supports the hypothesis of the neurological evolution of the mammalian lineage starting with a trend for an increase of the olfactory bulbs, which is associated with adaptations in the nasal cavity. This trend is suggested to be linked to the selective pressures for small-sized faunivorous, and probably nocturnal, animals, and represents an initial improvement of the sensory receptor system, subsequently leading to further development of the ‘superior’ structures for sensorial processing and integration.     

Digital Reconstruction of the Otic Region and Inner Ear of the Non-Mammalian Cynodont Brasilitherium riograndensis (Late Triassic, Brazil) and Its Relevance to the Evolution of the Mammalian Ear

The external anatomy of the petrosal, the bony labyrinth of the inner ear, and the stapes of Brasilitherium riograndensis (specimen UFRGS-PV-1043-T) were investigated by digital 3D reconstructions based on μCT scan images. Brasilitherium is the most basal taxon bearing a distinct promontorium, although less inflated than that of Morganucodon and still lacking a flat medial facet. A bony wall formed by the petrosal separates the cochlear canal and the vestibule from the brain cavity, with an internal acoustic meatus bearing distinct foramina for the facial nerve (VII) and vestibulocochlear nerve (VIII). The semicircular canals are irregular in shape, the anterior canal being the largest and the lateral one the smallest. Brasilitherium has an elongated but straight cochlear canal. The stapes resembles the morphology of derived non-mammaliaform cynodonts, such as Probainognathus and Pachygenelus, and differs from Thrinaxodon. By the allometric relationship of the cochlear canal and the estimated body mass, Brasilitherium can be grouped with Yunnanodon and Morganucodon in a regression line, which is below the line of mammals and above the line of non-avian reptiles. Brasilitherium fits in a sequence of gradual elongation of the cochlear canal associated with the enhancement in the capacity to hear higher frequencies. Among the constraints that might have triggered these transformations in small, insectivorous, and possibly nocturnal Mesozoic cynodont taxa is the improvement of detecting acoustically active insects.     

Virtual reconstruction of cranial endocasts of traversodontid cynodonts (Eucynodontia: Gomphodontia) from the upper Triassic of Southern Brazil

The brain endocasts of the late Triassic (Carnian) traversodontids (Eucynodontia: Gomphodontia) Siriusgnathus niemeyerorum and Exaeretodon riograndensis from southern Brazil are described based on virtual models generated using computed tomography scan data. Their skull anatomy resembles that of other non-mammaliaform cynodonts, showing an endocranial cavity that is not fully ossified. A “V-shaped” orbitosphenoid, neither fully developed nor ossified is present in E. riograndensis. The nasal cavity is confluent with the encephalic cavity. Thus, the anterior limit of the olfactory bulbs is not definite. The brain endocast is elongated, being narrow anteriorly and wide posteriorly, with the maximum width at the parafloccular cast. The olfactory bulbs do not present a clear division between their counterparts, due to the absence of a longitudinal sulcus. A longitudinal sulcus in the forebrain delimiting the cerebral hemispheres, the pineal tube, and the parietal foramen are absent in both taxa. The large and well-developed unossified zone is partially separated from the remaining endocast by a notch formed by the supraoccipital. The encephalization quotients, as well as the endocranial volume/body mass relationships of S. niemeyerorum and E. riograndensis are within the range expected for non-mammaliaform Therapsida.     

Origin and relationships of the Ictidosauria to non-mammalian cynodonts and mammals

Abstract

Ictidosaurian genera are allocated to two families, Tritheledontidae and Therioherpetidae. This paper provides a diagnosis for Ictidosauria. The previously named family Brasilodontidae is shown to be a junior synonym of a family, Therioherpetidae. It is concluded that Ictidosauria originated from Late Permian procynosuchid non-mammalian cynodonts rather than from Middle Triassic probainognathid non-mammalian cynodonts. The structure of the skull and jaws of a derived traversodontid Ischignathus sudamericanus from the early Late Triassic of Argentina supports an earlier view that tritylodontids are more closely related to traversodontid than probainognathid non-mammalian cynodonts. Tritylodontids should not be included in Ictidosauria, nor should they considered to be a sister group to mammaliaforms.     

The oldest cynodont: new clues on the origin and early diversification of the Cynodontia

Early mammaliaforms and their extinct relatives, nonmammaliaform cynodonts, have long been the focus of intense research in attempting to unravel how and when major changes toward mammalness occurred. The earliest well-known representatives of cynodonts are latest Late Permian in age. Here, we describe Charassognathus gracilis gen. et sp. nov. , from the early Late Permian of South Africa, representing the oldest cynodont yet found. This specimen displays a notch on the dentary in the same location as the base of the masseteric fossa in the basal cynodonts Procynosuchus and Dvinia , and represents the first indication in theriodonts of an invasion of occlusal musculature onto the dentary. A phylogenetic analysis of seven therocephalians and ten non-mammaliaform cynodonts and equally weighted characters resulted in nine most parsimonious trees, the strict consensus of which shows a basal polytomy in cynodonts, including Charassognathus , Dvinia , Procynosuchus and a clade including the remaining cynodonts. The basal polytomy in the majority rule consensus tree is reduced, as Procynosuchus and Dvinia form a clade. One most parsimonious tree, from an analysis using implied weights, positions Charassognathus as the most basal cynodont. This result implies that the Cynodontia initially diversified in Permian Gondwana, in what is now southern Africa.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 149 , 477–492.     

Osteohistology of the non-mammaliaform traversodontids Protuberum cabralense and Exaeretodon riograndensis from southern Brazil

Abstract

The current study presents a detailed analysis of the osteohistology of the Triassic non-mammaliaform traversodontid cynodonts Protuberum cabralense and Exaeretodon riograndesis. The data provided here adds new information on the growth patterns of South American traversodontids. A single subadult individual of P. cabralense revealed bone tissues comprising uninterrupted fibrolamellar bone. Patches of slower growing lamellar bone at the periphery of one of the elements suggests a transition to overall slower growth in later ontogeny. The bone tissues of E. riograndensis also exhibit uninterrupted fibrolamellar bone during early ontogeny, but growth became cyclical from mid-ontogeny. The early rapid, sustained growth observed in these taxa is similar to that seen in other traversodontids, and may be related to the achievement of large body size in the derived members of the clade.     

Virtual reconstruction and description of the cranial endocast of Pristerodon mackayi (Therapsida,Anomodontia)

The cranial endocast of Pristerodon mackayi is described, which has been virtually reconstructed on the basis of neutron tomographic data. The gross anatomy of the cranial endocast of Pristerodon resembles other nonmammalian synapsids such as Thrinaxodon liorhinus in having a narrow, tubular forebrain, well developed olfactory bulbs, a large parietal foramen and unossified zone. As it is the case in cynodonts the hindbrain of Pristerodon is broader than the mid‐ and forebrain. Large paraflocculi are developed. The medulla oblongata can be well distinguished from the pons. The pons is divided by a median ridge into two portions. There is no evidence for a neocortex, which seems to be also reflected in the low encephalization quotient of 0.18 estimated according to the method of Eisenberg. J. Morphol. 276:1089–1099, 2015. © 2015 Wiley Periodicals, Inc.     

Large tetrapod burrows from the Middle Triassic of Argentina: a behavioural adaptation to seasonal semi‐arid climate?

Krapovickas, V., Mancuso, A.C., Marsicano, C.A., Domnanovich, N.S. & Schultz, C.L. 2013: Large tetrapod burrows from the Middle Triassic of Argentina: a behavioural adaptation to seasonal semi‐arid climate? Lethaia, Vol. 46, pp. 154–169. We report the discovery of large burrow casts in the early Middle Triassic Tarjados Formation, at Talampaya National Park, north‐western Argentina. Facies analysis indicates the burrows are preserved in sandbars deposited by an ephemeral river under semi‐arid and seasonal climatic conditions. The structures are mostly preserved in longitudinal cross‐section and consist of an opening, an inclined tunnel (ramp), and a terminal chamber. The ramp is 8–14 cm in height, up to 130 cm in length and penetrates 49–63 cm bellow the palaeosurface with an inclination of 22°–30°. We studied burrow cast dimensions, overall architectural morphology, surficial marks, and compared them with other large burrows of both invertebrate and vertebrate origin. A tetrapod origin of the burrow casts was established based on: distinctive architecture, and size, which is more than twice the most common size range for large terrestrial invertebrate burrows. Comparison with other Upper Permian and Triassic tetrapod burrows allows us to identify three general morphological groups: (1) simple inclined burrows; (2) helical burrows; and (3) burrow network complexes, representing different behaviours. A study of tetrapod body fossils preserved within other Upper Permian and Triassic burrows shows that the Tarjados structures were most likely produced by non‐mammalian cynodonts. The environmental and climatic context suggests that aridity and seasonality played a fundamental role selecting burrowing behaviour in therapsids and that by the Early–Middle Triassic their burrowing behaviour attained a complexity comparable to modern mammals. □Argentina, behaviour, palaeoclimate, Permo‐Triassic, Tarjados Formation, Tetrapod burrows.     

Brain – Endocast Relationship in the Australian Lungfish,Neoceratodus forsteri,Elucidated from Tomographic Data (Sarcopterygii: Dipnoi)

Although the brains of the three extant lungfish genera have been previously described, the spatial relationship between the brain and the neurocranium has never before been fully described nor quantified. Through the application of virtual microtomography (μCT) and 3D rendering software, we describe aspects of the gross anatomy of the brain and labyrinth region in the Australian lungfish, Neoceratodus forsteri and compare this to previous accounts. Unexpected characters in this specimen include short olfactory peduncles connecting the olfactory bulbs to the telencephalon, and an oblong telencephalon. Furthermore, we illustrate the endocast (the mould of the internal space of the neurocranial cavity) of Neoceratodus, also describing and quantifying the brain-endocast relationship in a lungfish for the first time. Overall, the brain of the Australian lungfish closely matches the size and shape of the endocast cavity housing it, filling more than four fifths of the total volume. The forebrain and labyrinth regions of the brain correspond very well to the endocast morphology, while the midbrain and hindbrain do not fit so closely. Our results cast light on the gross neural and endocast anatomy in lungfishes, and are likely to have particular significance for palaeoneurologists studying fossil taxa.     

New information about <Emphasis Type="Italic">Irajatherium hernandezi</Emphasis> Martinelli,Bonaparte, Schultz &; Rubert 2005 (Eucynodontia,Tritheledontidae) from the upper triassic (Caturrita Formation,Paraná Basin) of Brazil

In this contribution, new specimens of the tritheledontid eucynodont Irajatherium hernandezi, from the Late Triassic (Caturrita Formation) of southern Brazil, are analyzed. The new material provides significant information about incisor count, canine size and shape, basicranial morphology, and other previously unknown aspects of skull and dentition. A cladistic analysis with inclusion of the new data supports the assignment of Irajatherium to Tritheledontidae, basal to Chalimininae and Pachygenelinae. Previously unknown characters of Irajatherium revealed by the new material include: the presence of three lower incisors; the first lower incisor is enlarged; the presence of large upper and lower canines with deep paracanine fossa on the maxilla; almost complete upper and lower postcanine tooth row with a pattern similar to that of other tritheledontids (e.g. Pachygenelus and Chaliminia); there is a conspicuous crest on the inner surface of the maxilla for the attachment of the inferred maxillary turbinates; partially confluent jugular foramen and fenestra rotunda within the jugular fossa, separated by a finger-like projection of the posterolateral wall of the opisthotic; and hypoglossal foramina located outside the jugular fossa. Irajatherium is a key taxon for understanding the early evolution of ictidosaurs, a group of cynodonts closely related to mammaliaforms, during the cynodont–mammal transition from the Late Triassic to Early Jurassic.     

Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear

The middle ear bones of Mesozoic mammals are rarely preserved as fossils and the morphology of these ossicles in the earliest mammals remains poorly known. Here, we report the stapes and incus of the euharamiyidan Arboroharamiya from the lower Upper Jurassic (～160 Ma) of northern China, which represent the earliest known mammalian middle ear ossicles. Both bones are miniscule in relation to those in non‐mammalian cynodonts. The skull length/stapedial footplate diameter ratio is estimated as 51.74 and the stapes length as the percentage of the skull length is 4%; both numbers fall into the stapes size ranges of mammals. The stapes is “rod‐like” and has a large stapedial foramen. It is unique among mammaliaforms in having a distinct posterior process that is interpreted as for insertion of the stapedius muscle and homologized to the ossified proximal (stapedial) end of the interhyal, on which the stapedius muscle attached. The incus differs from the quadrate of non‐mammalian cynodonts such as morganucodontids in having small size and a slim short process. Along with lack of the postdentary trough and Meckelian groove on the medial surface of the dentary, the ossicles suggest development of the definitive mammalian middle ear (DMME) in Arboroharamiya. Among various higher‐level phylogenetic hypotheses of mammals, the one we preferred places “haramiyidans” within Mammalia. Given this phylogeny, development of the DMME took place once in the allotherian clade containing euharamiyidans and multituberculates, probably independent to those of monotremes and therians. Thus, the DMME has evolved at least three times independently in mammals. Alternative hypothesis that placed “haramiyidans” outside of Mammalia would require independent acquisition of the DMME in multituberculates and euharamiyidans as well as parallel evolution of numerous derived similarities in the dentition, occlusion pattern, mandibles, cranium, and postcranium between the two groups and between “haramiyidans” and other mammals. J. Morphol. 279:441–457, 2018. © 2016 Wiley Periodicals, Inc.     

Growth patterns as deduced from bone microstructure of some selected neotherapsids with special emphasis on dicynodonts: Phylogenetic implications

Osteohistological analysis of the dicynodonts Endothiodon, Diictodon, Lystrosaurus and Wadiasaurus reveals distinctly different growth patterns within a framework of an overall fast growth. The late Permian endemic taxon from India, Endothiodon mahalanobisi and the South African Diictodon feliceps had periodic fast growth. The early Triassic Lystrosaurus murrayi and the middle Triassic Wadiasaurus indicus had an initial fast growth followed by a relatively slow growth later in ontogeny as is observed from the presence of peripheral parallel fibred bone. Although all examined dicynodont genera had an indeterminate growth strategy, the bone microstructure of Wadiasaurus suggests that its growth was much slower than that of other dicynodonts examined. Mapping of osetohistological character states on a cladogram depicting the inter-relationship between available neotherapsid genera shows that fibrolamellar bone tissue, overall fast growth and indeterminate growth strategy were plesiomorphic for the neotherapsids. A considerable reduction in developmental plasticity and evolution of apparently independent growth trajectories from environmental conditions are evident within the non-mammalian cynodonts, with the advanced tritylodontids achieving almost a mammalian growth trajectory.     

Enigmatic teeth from the Jurassic–Cretaceous transition of Morocco: The latest known non-mammaliaform cynodonts (Synapsida,Cynodontia) from Africa?

Two tooth morphotypes corresponding to one or two tetrapod species from the Late Jurassic or Earliest Cretaceous locality of Ksar Metlili (KM), Anoual Syncline (eastern Morocco), are reported and described. These teeth cannot be related to any of the identified vertebrate major groups of this site. They are tricusped and uniradiculate, with a high and large main central cusp mesio-distally surrounded by two smaller accessory cusps. Their morphology is reminiscent of several taxa such as pterosaurs, notosuchians and mammals, with which they are compared here. These morphotypes are tentatively referred to cf. Cynodontia indet. They would be the most recent non-mammaliaform cynodonts reported in Africa and among the latest described. The KM specimens display remarkable plesiomorphic dental features with respect to known contemporaneous non-mammaliaform cynodonts. They might indicate the survival of a relict lineage in a North African refugium.     

First 'Rauisuchian' archosaur (Pseudosuchia,Loricata) for the Middle Triassic Santacruzodon Assemblage Zone (Santa Maria Supersequence), Rio Grande do Sul State,Brazil

The ‘Rauisuchia’ are a group of Triassic pseudosuchian archosaurs that displayed a near worldwide distribution. In Brazil, their fossils are found only in the Santa Maria Formation (Paraná Basin) of the Rio Grande do Sul State, specifically in the Middle Triassic Dinodontosaurus assemblage zone (AZ) and the Late Triassic Hyperodapedon AZ (Rauisuchus tiradentes). Between these two cenozones is the Santacruzodon AZ (Middle Triassic), whose record was, until now, restricted to non-mammalian cynodonts and the proterochampsian Chanaresuchus bonapartei. Here we present the first occurrence of a rauisuchian archosaur for this cenozone, from the Schoenstatt outcrop, located near the city of Santa Cruz do Sul and propose a new species, based on biostratigraphical evidence and a comparative osteological analysis.     

Morphology and postnatal ontogeny of the cranial endocast and paranasal sinuses of capybara (Hydrochoerus hydrochaeris), the largest living rodent

Recent studies have analyzed and described the endocranial cavities of caviomorph rodents. However, no study has documented the changes in the morphology and relative size of such cavities during ontogeny. Expecting to contribute to the discussion of the endocranial spaces of extinct caviomorphs, we aimed to characterize the cranial endocast morphology and paranasal sinuses of the largest living rodent, Hydrochoerus hydrochaeris, by focusing on its ontogenetic growth patterns. We analyzed 12 specimens of different ontogenetic stages and provided a comparison with other cavioids. Our study demonstrates that the adult cranial endocast of H. hydrochaeris is characterized by olfactory bulbs with an irregular shape, showing an elongated olfactory tract without a clear circular fissure, a marked temporal region that makes the endocast with rhombus outline, and gyrencephaly. Some of these traits change as the brain grows. The cranial pneumatization is present in the frontal and lacrimal bones. We identified two recesses (frontal and lacrimal) and one sinus (frontal). These pneumatic cavities increase their volume as the cranium grows, covering the cranial region of the cranial endocast. The encephalization quotient was calculated for each specimen, demonstrating that it decreases as the individual grows, being much higher in younger specimens than in adults. Our results show that the ontogenetic stage can be a confounding factor when it comes to the general patterns of encephalization of extinct rodents, reinforcing the need for paleobiologists to take the age of the specimens into account in future studies on this subject to avoid age-related biases.     

Evolution of the Brasilodontidae (Cynodontia-Eucynodontia)

The genera of the Brasilodontidae, Protheriodon, Brasilodon, Brasilitherium, Minicynodon and the Indian Panchetocynodon, are briefly summarised and the more significant evolutionary information from them is discussed. Brasilodon and Brasilitherium are possibly related to the origin of Kuehneotheridae and Morganucodontidae, respectively. A systematic rearrangement is proposed for the monophyletic Epicynodontia integrated by the subclades Brasilodontia, Gomphodontia and Galesauria. It is considered that Brasilodontia (Brasilodontidae and Tritheledontidae) have strong differences with the remaining cynodonts and are connected with the origin of mammals. It is recognised that Galesauridae, Thrinaxodontidae and Probainognathidae are only distantly related to the origin of mammals. Within the Brasilodontidae were not found any dental or mandibular character shared with the Haramiyavidae.