150 years of synapsid paleoneurology: the origins of the mammalian brain, behavior, sense organs and physiology
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Andrew D. Bolton, Taahirah Mangera and Julien Benoit
Abstract
A century and a half of paleoneurological study of synapsids has provided invaluable insight into the evolution of their brain, sense organs, behavior, and physiology. Here, we review and discuss the evidence for parental care, brooding, intraspecific combat, display, and gregariousness, and conclude that evidence for higher levels of social interactions and communication is piling up and may soon push the origin of sociality in the mammalian lineage to the middle Permian. We also review the paleoneurological cues (the trigeminal canals, parietal foramen, and inner ear) that support a new evolutionary hypothesis in which the homeogene MSX2 mutated early in the probainognathian cynodonts and changed their biology towards a more mammalian condition. This includes the loss of the parietal foramen, inflation of the cerebellar vermis, maintenance of a fur pelt, and appearance of mammary glands, some 247 million years ago. This was followed by the origin of the ability to whisk 241 million years ago, and that of endothermy 233 million years ago, as indicated by the evolution of the trigeminal and semicircular canals, respectively. Finally, we review the immense progress made in the study of encephalization and support that probainognathians went through a neurosensory revolution during the Triassic. Their newly acquired small body size, fur, and nocturnal lifestyle generated sensory input that affected the evolution of all their sensory organs, leading up to the development of the modern mammalian brain.
Non-technical Summary
Permo-Triassic synapsids are the ancestors of mammals. Study of the synapsid brain is 150 years old and is reviewed here. Some evidence supports that mammalian ancestors have been capable of complex behavior such as parental care, brooding, intraspecific combat, display, and gregariousness for up to 265–260 million years. The study of the brain and sense organs supports that they evolved hair and warm blood 240–230 million years ago. Brain evolution was driven by a neurosensory revolution during the Triassic as terrestrial ecosystems began to be ruled by archosaurs.
Introduction
The non-mammalian synapsids (or stem mammals, hereafter referred to as the synapsids) are the biologically reptilian-like ancestors of mammals. They form a paraphyletic assemblage of highly diverse taxa at the evolutionary stem of the mammalian clade (Fig. 1). They represent one of the earliest evolutionary radiations of terrestrial amniotes during the late Paleozoic and early Mesozoic that encompassed a wide variety of body sizes (from shrew- to rhinoceros-sized animals), diets (scavengers, predators, insectivores, and high- and low-level herbivores), and locomotory modes (including fast and slow terrestrial, as well as semi-aquatic, fossorial, and arboreal species) (Cox, Reference Cox, Joysey and Kemp1972; Rubidge and Sidor, Reference Rubidge and Sidor2001; Canoville and Laurin, Reference Canoville and Laurin2010; Fröbisch and Reisz, Reference Fröbisch and Reisz2011; Angielczyk and Kammerer, Reference Angielczyk, Kammerer, Zachos and Asher2018; Spindler et al., Reference Spindler, Werneburg, Schneider, Luthardt, Annacker and Rößler2018; Bhat et al., Reference Bhat, Shelton and Chinsamy2022; Singh et al., Reference Singh, Elsler, Stubbs, Rayfield and Benton2024). From the late Carboniferous to the Late Triassic, the synapsids were the dominant land animals, as is reflected by their abundant fossils in rocks of this time interval (MacRae, Reference MacRae1999; Angielczyk and Kammerer, Reference Angielczyk, Kammerer, Zachos and Asher2018).
Figure 1. Simplified phylogeny of Synapsida modified from Benoit et al. (Reference Benoit, Dollman, Smith and Manger2023b). Following Benoit et al. (Reference Benoit, Dollman, Smith and Manger2023b), as well as other authors in the field of synapsid paleoneurology (e.g., Jerison, Reference Jerison1973; Quiroga, Reference Quiroga1979, Reference Quiroga1984; Rowe et al., Reference Rowe, Macrini and Luo2011), the classification of Synapsida is here simplified into a series of successive grades (paraphyletic assemblages of taxa). Accordingly, the terms synapsids, therapsids, cynodonts, probainognathians, and early mammaliaforms are used as grades (rather than clades) in the text.
Despite the long list of osteological characters that set clade Mammalia apart, which form the baseline of our current understanding of the origin of mammals (Allin, Reference Allin1975; Kemp, Reference Kemp2005; Luo et al., Reference Luo, Schultz, Ekdale, Clack, Fay and Popper2016; Maier and Ruf, Reference Maier and Ruf2016; Norton et al., Reference Norton, Abdala and Benoit2023), members of this clade are more commonly identified by soft tissue and physiological traits, the most quintessential of which are the enlarged brain and isocortex, complex behavior, prolonged parental care period, elevated metabolism (endothermy, hereafter used in the sense of non-shivering thermogenesis; Grigg et al., Reference Grigg, Nowack, Bicudo, Bal, Woodward and Seymour2022), and the presence of mammary glands and hair. Unfortunately, reconstructing how and when these defining mammalian traits evolved is notoriously challenging because soft tissue, physiological, and behavioral characters do not readily fossilize (Rowe, Reference Rowe1996; Rowe et al., Reference Rowe, Macrini and Luo2011; Lovegrove, Reference Lovegrove2019; Benton, Reference Benton2021; Benoit et al., Reference Benoit, Dollman, Smith and Manger2023b; Norton et al., Reference Norton, Abdala and Benoit2023).
Despite this, recent research efforts have been successful in tracing the origin and evolution of these traits because they are correlated directly to paleoneurological, endocranial, and sense organ-related osteological characters, which leave readily observable evidence on the fossilized skulls of synapsids (see Benoit et al., Reference Benoit, Dollman, Smith and Manger2023b; Norton et al., Reference Norton, Abdala and Benoit2023, for reviews). These had long been considered out of reach, but their study has been made possible by CT scanning imagery (X-ray, neutron, and synchrotron) and digital 3D modeling techniques to access hitherto out-of-reach paleoneurological characters.
Research on the origins of an enlarged brain (and associated isocortex and complex behavior), attuned sense organs, and endothermy have suggested that the origin of hair, whiskers, lactation, and typical mammalian behavior such as parental care and gregariousness most likely predated the origin of crown group Mammalia (Rowe et al., Reference Rowe, Macrini and Luo2011; Benoit et al., Reference Benoit, Dollman, Smith and Manger2023b; Norton et al., Reference Norton, Abdala and Benoit2023). This incidentally contributed to reshaping our understanding of the origin of “mammalness” and its deep evolutionary origins among their reptilian-like ancestors. The current contribution aims at summarizing these recent advances.
A brief history of synapsid paleoneurology
Brain evolution is traced through the fossil record by studying the internal cast of the brain cavity of fossilized skulls, usually referred to, more simply, as the endocranial cast or endocast (Jerison, Reference Jerison1973; de Sousa et al., Reference de Sousa, Beaudet, Calvey, Bardo and Benoit2023; Rowe, Reference Rowe, Dozo, Paulina-Carabajal, Macrini and Walsh2023). Study of the paleoneurology of synapsids began 150 years ago, in 1876, with the publication of the endocast of the cynodont grade (i.e., non-mammalian cynodonts; Fig. 1) species Nythosaurus larvatus Owen, Reference Owen1876, by Richard Owen (Fig. 2.1) (Owen, Reference Owen1876; Pusch et al., Reference Pusch, Kammerer, Fernandez and Fröbisch2022). For almost a hundred years, to access data on the synapsid nervous system, paleoneurologists had to rely on the slim chances of preservation of natural endocasts of neurosensory cavities and canals (e.g., Watson, Reference Watson1913; Cox and Broom, Reference Cox and Broom1962), complete preparation (e.g., Case, Reference Case1914; Tatarinov, Reference Tatarinov1965; Kemp, Reference Kemp1969, Reference Kemp1979), as well as on destructive methods such as sectioning, serial sectioning, and serial grinding (e.g., Sollas and Sollas, Reference Sollas and Sollas1913; Olson, Reference Olson1944; Boonstra, Reference Boonstra1968; see Benoit and Jasinoski, Reference Benoit and Jasinoski2016, for a review). In a rather unusual manner for the field, paleoneurologists studying synapsids have mostly relied upon natural endocasts or digital 3D reconstructions, but seldom made artificial endocasts using latex or plaster of Paris (Edinger, Reference Edinger1975).
Figure 2. Endocasts, in dorsal view, illustrating the history of techniques used in synapsid paleoneurology. (1) Natural endocast of Nythosaurus larvatus described by Owen (Reference Owen1876), NHMUK PV R 1715 from the Natural History Museum UK, courtesy of M. Day; (2) first digital endocast based on the CT-scanned skull of a Thrinaxodon liorhinus Seeley, Reference Seeley1894, published by Rowe et al. (Reference Rowe, Carlson, Bottorff and Olson1995) as a Compact Disc; (3) digital endocast based on synchrotron data of Thrinaxodon liorhinus by Fernandez et al. (Reference Fernandez, Abdala, Carlson, Cook, Rubidge, Yates and Tafforeau2013). Endocasts not to scale.
For most of the twentieth century, data were scarce and progress was slow, yet steady, mostly thanks to the noted contributions of Harry J. Jerison (Reference Jerison1973), who introduced the Encephalization Quotient as a measure of relative brain size, Zofia Kielan-Jaworowska for her work on Mesozoic mammal paleoneurology (Kielan-Jaworowska, Reference Kielan-Jaworowska1983, Reference Kielan-Jaworowska1984), and Juan C. Quiroga, who described the endocast of many non-mammaliaform cynodonts in the late 1970s and early 1980s (see Jerison, Reference Jerison1973; Edinger, Reference Edinger1975; Hopson et al., Reference Hopson, Gans, Northcutt, Ulinski, Gans, Northcutt and Ulinski1979; Kielan-Jaworowska et al., Reference Kielan-Jaworowska, Cifelli and Luo2004; Kerber et al., Reference Kerber, Roese-Miron, Bubadué and Martinelli2024a, for reviews).
Progress was slowed, in large part, by lack of ossification of the synapsid braincase, particularly on its ventral and lateral aspects (Kielan-Jaworowska et al., Reference Kielan-Jaworowska, Cifelli and Luo2004; Kemp, Reference Kemp2009; Benoit et al., Reference Benoit, Jasinoski, Fernandez and Abdala2017a). Early synapsids, with a few exceptions such as the dinocephalians, biarmosuchians, and Kawingasaurus (Benoit et al., Reference Benoit, Fernandez, Manger and Rubidge2017b; Laaß and Kaestner, Reference Laaß and Kaestner2017), lack a laterally expanded epipterygoid and an ossified cribriform plate anteriorly. Dorsally, the internal surface of the supraoccipital is excavated by a deep unossified zone (like in modern turtles, in which it is filled up by cartilage; Werneburg et al., Reference Werneburg, Evers and Ferreira2021), and ventrally, below the olfactory bulbs, the more or less ossified orbitosphenoids are floating as part of the mostly cartilaginous median septum (Benoit et al., Reference Benoit, Jasinoski, Fernandez and Abdala2017a).
The process of ossification of the braincase began in probainognathian cynodonts only and was achieved in early Mammaliaformes (Kielan-Jaworowska et al., Reference Kielan-Jaworowska, Cifelli and Luo2004; Benoit et al., Reference Benoit, Jasinoski, Fernandez and Abdala2017a; Norton et al., Reference Norton, Abdala and Benoit2023). The ventral flexure of the brain (Benoit et al., Reference Benoit, Fernandez, Manger and Rubidge2017b) partly solved the long-lasting question of the ventral limits of the endocast in early synapsids (Kemp, Reference Kemp2009), but the lack of ossified walls and floor still poses major challenges to reconstructing the endocast, nerves, and blood vessels in many synapsid taxa (e.g., Laaß et al., Reference Laaß, Schillinger and Kaestner2017a; Bazzana et al., Reference Bazzana, Evans, Bevitt and Reisz2022; Bazzana-Adams et al., Reference Bazzana-Adams, Evans and Reisz2023).
Synapsid paleoneurology was revived with the application of new imaging techniques such as microcomputed tomography (CT) scanning using X-ray, synchrotron, or neutron beams to create a series of digital slices of fossilized skulls. These images are processed in silico to extract the 3D volume of the normally out-of-reach brain cavity (endocast), inner ear (bony labyrinth), and other nervous structures (such as the maxillary canal of the trigeminal nerve) through a process called segmentation. The first CT-scanned synapsid was a Thrinaxodon skull in 1993 (Fig. 2.2), which was shortly preceded by the CT scanning of the skull of the early mammaliaform Morganucodon (Luo and Ketten, Reference Luo and Ketten1991; Rowe et al., Reference Rowe, Carlson, Bottorff and Olson1995; Rowe, Reference Rowe1996). The subsequent spread of CT scanning (mostly X-ray-based CT scanning) in paleontology labs globally provided access to an unprecedented quantity of synapsid, early mammaliaform, and Mesozoic mammal endocranial data (e.g., Hurum, Reference Hurum1998; Macrini, Reference Macrini2006; Macrini et al., Reference Macrini, Rougier and Rowe2007; Luo et al., Reference Luo, Ruf, Schultz and Martin2011; Rowe et al., Reference Rowe, Macrini and Luo2011; Rodrigues et al., Reference Rodrigues, Ruf and Schultz2014; Laaß, Reference Laaß2015a, Reference Laaßb; Maier and Ruf, Reference Maier and Ruf2016; Benoit et al., Reference Benoit, Fernandez, Manger and Rubidge2017b, Reference Benoit, Manger, Fernandez and Rubidgec; Laaß and Kaestner, Reference Laaß and Kaestner2017; Laaß et al., Reference Laaß, Schillinger and Kaestner2017a; Rodrigues et al., Reference Rodrigues, Martinelli, Schultz, Corfe, Gill, Soares and Rayfield2018; Pavanatto et al., Reference Pavanatto, Kerber and Dias‐da‐Silva2019; Hoffmann et al., Reference Hoffmann, Rodrigues, Soares and Andrade2021; Araújo et al., Reference Araújo, Macungo, Fernandez, Chindebvu and Jacobs2022a; Bazzana-Adams et al., Reference Bazzana-Adams, Evans and Reisz2023; Rowe, Reference Rowe, Dozo, Paulina-Carabajal, Macrini and Walsh2023; Kerber et al., Reference Kerber, Roese-Miron, Bubadué and Martinelli2024a; Pusch et al., Reference Pusch, Kammerer and Fröbisch2024; Medina et al., Reference Medina, Martinelli, Gaetano, Roese-Miron, Tartaglione, Backs, Novas and Kerber2025, and references therein), including studies of the inner ear (Luo and Ketten, Reference Luo and Ketten1991; Luo et al., Reference Luo, Ruf, Schultz and Martin2011; Rodrigues et al., Reference Rodrigues, Ruf and Schultz2014; Laaß, Reference Laaß2015a, Reference Laaßb; Benoit et al., Reference Benoit, Manger, Fernandez and Rubidge2017c; Araújo et al., Reference Araújo, David, Benoit, Lungmus and Stoessel2022b; Bazzana et al., Reference Bazzana, Evans, Bevitt and Reisz2022; Bazzana-Adams et al., Reference Bazzana-Adams, Evans and Reisz2023) and trigeminal nerves (Benoit et al., Reference Benoit, Manger and Rubidge2016a, Reference Benoit, Manger, Fernandez and Rubidgeb, Reference Benoit, Abdala, Manger and Rubidgec, Reference Benoit, Angielczyk, Miyamae, Manger, Fernandez and Rubidge2018, Reference Benoit, Ruf, Miyamae, Fernandez, Rodrigues and Rubidge2020a, Reference Benoit, Legendre, Farke, Neenan, Mennecart, Costeur, Merigeaud and Mangerb, Reference Benoit, Norton and Jirah2023a; Laaß and Kaestner, Reference Laaß and Kaestner2017; Wallace et al., Reference Wallace, Martínez and Rowe2019; Muchlinski et al., Reference Muchlinski, Wible, Corfe, Sullivan and Grant2020; Duhamel et al., Reference Duhamel, Benoit, Rubidge and Liu2021; Bazzana et al., Reference Bazzana, Evans, Bevitt and Reisz2023; Norton et al., Reference Norton, Abdala and Benoit2023; Fonseca et al., Reference Fonseca, Martinelli, Gill, Rayfield, Schultz, Kerber, Ribeiro and Soares2024a; Miyamae et al., Reference Miyamae, Benoit, Ruf, Sibiya and Bhullar2024; Pusch et al., Reference Pusch, Kammerer and Fröbisch2024).
Subsequent synchrotron (Fig. 2.3) and neutron imaging enabled data extraction from the most challenging, largest, or most metallic nodule-rich specimens (Laaß et al., Reference Laaß, Schillinger and Werneburg2017b; von der Heyden et al., Reference von der Heyden, Benoit, Fernandez and Roychoudhury2020) so that the dataset of synapsid endocasts has now grown to almost 60 genera (Table 1).
Figure 3. Short- and long-term consequences of head butting in tapinocephalid dinocephalians. (1) Routes through the braincase and to the neck taken by the energy of a head-on impact, around the endocast (left) and on the surface of the skull (right). (2) Distribution of cranial pathologies in tapinocephalid dinocephalians (left) compared to the stress distribution resulting from the finite element analysis (FEA, high stress in red) simulation of head butting (top, lateral view; bottom, dorsal views). (3) Digital cross-section through the braincase of a Moschognathus (AM 4950) showing the presence of an abscess (left) and two magnifications of the abscess area (right). (4) Interpretive drawing of (3) comparing the position of the abscess (left side of the skull) to the route taken by a head-on impact on the fighting surface (right side of the skull). Abbreviations: Abs = abscess; Bas = basicranium; Heal = healing bone tissue; Drain = pus drainage canal; FS = fighting surface; Osp = orbitosphenoid. Red arrows indicate the route taken by the energy of the impact. (1) and (2) not to scale.
Figure 4. Illustration of the hypothesized trade-off between the size of the canine and cranial adaptations to head-butting in mid-Permian dinocephalians (1), the skull of modern ruminants (2), and pictures of modern cervids (3). (1, 2) Orientation of the braincase (marked by the orientation of the lateral semicircular canal of the inner ear) in dinocephalians (1) from left to right: Anteosaurus, Moschognathus, and a derived tapinocephalid indet., and modern ruminants (2) from left to right: Moschus, Muntiacus, and Connochaetes; transparent skulls aligned on the plane of their lateral semicircular canal (white dashed line). (3) Pictures of living cervids in lateral view (from left to right: Hydropotes, Muntiacus, and Cervus). LSC = lateral semicircular canal. Not to scale.
