The neuroanatomy of hadrosaurid dinosaurs is well known from North America and Asia.In Europe only a few cranial remains have been recovered that include the braincase.Arenysaurus is the first European endocast for which the paleoneuroanatomy has been studied.The resulting data have enabled us to draw ontogenetic, phylogenetic and functional inferences.Arenysaurus preserves the endocast and the inner ear.This cranial material was CT-scanned, and a 3D-model was generated.The endocast morphology supports a general pattern for hadrosaurids with some characters that distinguish it to a subfamily level, such as a brain cavity that is anteroposteriorly shorter or the angle of the major axis of the cerebral hemisphere to the horizontal in lambeosaurines.Both these characters are present in the endocast of Arenysaurus.Osteological features indicate an adult ontogenetic stage while some paleoneuroanatomical features are indicative of a subadult ontogenetic stage.It is hypothesized that the presence of puzzling mixture of characters that suggest different ontogenetic stages for this specimen may reflect some degree of dwarfism in Arenysaurus.Regarding the inner ear, its structure shows differences from the ornithopod clade with respect to the height of the semicircular canals.These differences could lead to a decrease in the compensatory movements of eyes and head, with important implications for the paleobiology and behavior of hadrosaurid taxa such as Edmontosaurus, Parasaurolophus and Arenysaurus.The endocranial morphology of European hadrosaurids sheds new light on the evolution of this group and may reflect the conditions in the archipelago where these animals lived during the Late Cretaceous.
Abstract Therapsids were a dominant component of middle–late Permian terrestrial ecosystems worldwide, eventually giving rise to mammals during the early Mesozoic. However, little is currently known about the time and place of origin of Therapsida. Here we describe a definitive therapsid from the lower–?middle Permian palaeotropics, a partial skeleton of a gorgonopsian from the island of Mallorca, western Mediterranean. This specimen represents, to our knowledge, the oldest gorgonopsian record worldwide, and possibly the oldest known therapsid. Using emerging relaxed clock models, we provide a quantitative timeline for the origin and early diversification of therapsids, indicating a long ghost lineage leading to the evolutionary radiation of all major therapsid clades within less than 10 Myr, in the aftermath of Olson’s Extinction. Our findings place this unambiguous early therapsid in an ancient summer wet biome of equatorial Pangaea, thus suggesting that the group originated in tropical rather than temperate regions.
Article Figures and data Abstract eLife digest Introduction Results Discussion Materials and methods Appendix 1 Appendix 2 Appendix 3 Data availability References Decision letter Author response Article and author information Metrics Abstract Flying squirrels are the only group of gliding mammals with a remarkable diversity and wide geographical range. However, their evolutionary story is not well known. Thus far, identification of extinct flying squirrels has been exclusively based on dental features, which, contrary to certain postcranial characters, are not unique to them. Therefore, fossils attributed to this clade may indeed belong to other squirrel groups. Here we report the oldest fossil skeleton of a flying squirrel (11.6 Ma) that displays the gliding-related diagnostic features shared by extant forms and allows for a recalibration of the divergence time between tree and flying squirrels. Our phylogenetic analyses combining morphological and molecular data generally support older dates than previous molecular estimates (~23 Ma), being congruent with the inclusion of some of the earliest fossils (~36 Ma) into this clade. They also show that flying squirrels experienced little morphological change for almost 12 million years. https://doi.org/10.7554/eLife.39270.001 eLife digest Mammals can walk, hop, swim and fly; a few, like marsupial sugar gliders or colugos, can even glide. With 52 species scattered across the Northern hemisphere, flying squirrels are by far the most successful group that adopted this way of going airborne. To drift from tree to tree, these small animals pack their own ‘parachute’: a membrane draping between their lower limbs and the long cartilage rods that extend from their wrists. Tiny specialized wrist bones, which are unique to flying squirrels, help to support the cartilaginous extensions. The origin of flying squirrels is a point of contention: while most genetic studies point towards the group splitting from tree squirrels about 23 million years ago, the oldest remains – mostly cheek teeth – suggest the animals were already soaring through forests 36 million years ago. However, recent studies show that the dental features used to distinguish between gliding and non-gliding squirrels may actually be shared by the two groups. In 2002, the digging of a dump site in Barcelona unearthed a peculiar skeleton: first a tail and two thigh bones, big enough that the researchers thought it could be the fossil of a small primate. In fact, and much to the disappointment of paleoprimatologists, further excavating revealed that it was a rodent. As the specimen – nearly an entire skeleton – was being prepared, paleontologists insisted that all the ‘dirt’ attached to the bones had to be carefully screen-washed. From the mud emerged the minuscule specialized wrist bones: the primate-turned-rodent was in fact Miopetaurista neogrivensis, an extinct flying squirrel. Here, Casanovas-Vilar et al. describe the 11.6 million years old fossil, the oldest ever found. The wrist bones reveal that the animal belongs to the group of flying squirrels that have large sizes. Evolutionary analyses that combined molecular and paleontological data demonstrated that flying squirrels evolved from tree squirrels as far back as 31 to 25 million years ago, and possibly even earlier. In addition, the results show that Miopetaurista is closely related to Petaurista, a modern group of giant flying squirrels. In fact, their skeletons are so similar that the large species that currently inhabit the tropical and subtropical forests of Asia could be considered living fossils. Molecular and paleontological data are often at odds, but this fossil shows that they can be reconciled and combined to retrace history. Discovering older fossils, or even transitional forms, could help to retrace how flying squirrels took a leap from the rest of their evolutionary tree. https://doi.org/10.7554/eLife.39270.002 Introduction Flying squirrels (Sciurinae, Pteromyini) are the only group of gliding mammals to have achieved a significant diversity (52 species in 15 genera) and wide geographical distribution across Eurasia and North America (Koprowski et al., 2016). They have been classically regarded as a distinct subfamily among the Sciuridae (McKenna and Bell, 1997; McLaughlin, 1984; Simpson, 1945), and even sometimes considered a separate family derived from a different group than the remaining sciurids (De Bruijn and Ünay, 1989; Forsyth Major, 1893; Mein, 1970). The fact that presumed fossil flying squirrels are at least as old as (or maybe even older than) the oldest tree squirrels (36.6 – 35.8 Ma) may support the latter hypothesis. However, flying squirrels are currently recognized as a monophyletic clade, as supported by a set of synapomorphies in the wrist (Thorington, 1984). The carpal anatomy of flying squirrels is unique, being related to the structures that support the patagium and their particular gliding position, which is different from that of all other gliding mammals (Thorington, 1984; Thorington and Darrow, 2000). Molecular phylogenies indicate that flying squirrels (tribe Pteromyini) are nested within tree squirrels (subfamily Sciurinae) and likely diverged as recently as the latest Oligocene–early Miocene (23 ± 2.1 Ma) (Fabre et al., 2012; Mercer and Roth, 2003; Steppan et al., 2004). Notwithstanding, the pteromyin fossil record suggests a much older split. Indeed, one of the earliest sciurids, Hesperopetes thoringtoni from the late Eocene (36.6 – 35.8 Ma) of North America, has been related to the lineage leading to flying squirrels according to dental morphology (Emry and Korth, 2007). In the light of molecular results, it was conceded that Hesperopetes unlikely represented a pteromyin and was not assigned to any squirrel subfamily (Emry and Korth, 2007). On the other hand, this genus appears to have been closely related to Oligopetes (Emry and Korth, 2007), an earliest Oligocene (ca. 34 – 31 Ma) purported flying squirrel from Europe and Pakistan (Cuenca Bescós and Canudo, 1992; De Bruijn and Ünay, 1989; Heissig, 1979; Marivaux and Welcomme, 2003). Hesperopetes is last recorded during the earliest Oligocene (Orellan; Korth, 2017), coinciding with the oldest record of Sciurion (Bell, 2004), yet another alleged flying squirrel. Isolated cheek teeth are the only material available for all these taxa, which have been related to flying squirrels exclusively based on dental morphology. In fact, the whole fossil record of flying squirrels almost exclusively consists of isolated cheek teeth and a few mandibular and maxillary fragments. Unfortunately, dental features commonly used to recognize flying squirrels are not unique but also present in other sciurids (Thorington et al., 2005), so it is uncertain if any of the extinct ‘flying’ squirrels belonged to this group. Furthermore, if any of the oldest (late Eocene–early Oligocene) forms truly represented a pteromyin this would imply a discrepancy of more than 10 Myr between molecular and paleontological data. Contrary to dental material, postcranial remains do show diagnostic characters of the pteromyins (Thorington, 1984; Thorington et al., 2005; Thorington and Darrow, 2000). Therefore, they are of utmost importance to clarify the assignment of extinct ‘flying’ squirrels and calibrate their divergence date from other sciurids. Yet, these have not been described and are rarely preserved in the fossil record. Here we report a remarkably complete skeleton of a Miocene squirrel that displays the gliding-related diagnostic features shared by extant pteromyins and allows for a recalibration of the time of origin and diversification of the group. The fossil record of ‘flying’ squirrels is further discussed in the light of this new finding and the results of our phylogenetic analyses. Results Recovered material and specific attribution The described partial skeleton (IPS56468; Figure 1, Videos 1, 3D model in Supplementary file 1) was recovered at Abocador de Can Mata site ACM/C5-D1 (els Hostalets de Pierola, Catalonia, Spain; see Materials and Methods), with an estimated age of 11.63 Ma (Alba et al., 2017). The recovered remains were found partly articulated (Figure 2—figure supplement 1) and comprise more than 80 complete and fragmentary bones including the skull (Figure 6—figure supplement 1) and elements of the fore- and hindlimbs (Figures 2–5, Figure 2, Table 1). Additional material, including a second cranium (Figure 6—figure supplement 2), has been recovered from the same horizon and other roughly coeval ACM localities (Table 2). The specimens are assigned to Miopetaurista neogrivensis based on diagnostic cheek tooth morphology (Figure 3; for detailed description and comparisons of cheek teeth morphology see Appendix 3.1). In the ACM localities a second genus of ‘flying’ squirrel, Albanensia, is recorded, but Miopetaurista is clearly distinguished by its larger size, and several morphological features. The diagnostic characters of M. neogrivensis comprise: its large size; the presence of a complete entolophid and the frequent occurrence of a short mesolophid in the lower molars; and the large mesostyle in the P4 (Casanovas-Vilar et al., 2015; Mein, 1970). Miopetaurista neogrivensis has only been reported from La Grive L5 (type locality) and L3 in France, from Bellestar (Seu d’Urgell Basin, also in Catalonia), and from several sites from the Vallès-Penedès Basin (Casanovas-Vilar et al., 2015). This species is extremely rare, being represented by just a few isolated cheek teeth in most of the Vallès-Penedès sites. Figure 1 Download asset Open asset The fossil flying squirrel Miopetaurista neogrivensis. (a) Reconstruction of the skeleton based in the partial skeleton IPS56468 from Abocador de Can Mata. Missing elements are based on extant giant flying squirrel Petaurista petaurista and are colored in blue. (b) Life appearance of Miopetaurista neogrivensis showing the animal ready to land on a tree branch. Coat pattern and color are based in extant Petaurista species, the sister taxon of Miopetaurista (see Figure 7). See Video 1 for an animated version of this reconstruction and 3D model in Supplementary file 1 to view and manipulate a low-quality model of the skeleton. For recovered elements of the postcranial skeleton see Figures 2 and 4 and Table 1. For a description and comparison of the postcranial bones, see Appendix 3.3. See Figure 6 and Video 3 for a more detailed cranial reconstruction. 3D models generated from µCT scan data and photogrammetry. Scale bar is 4 cm. https://doi.org/10.7554/eLife.39270.003 Figure 2 with 1 supplement see all Download asset Open asset Selected postcranial elements of the partial skeleton of Miopetaurista neogrivensis. (a–b) Right humerus (IPS56468f) in cranial and caudal views. (c–d) Right femur (IPS56468b) in cranial and caudal views. (e–f) Right tibia (IPS56468a) in cranial and caudal views. (g–h) Lumbar vertebrae L3–L6 (IPS56468m–n) in dorsal and ventral views. Note that vertebrae are in anatomical connection. (i–j) Partial right coxal (IPS56468k) in lateral and medial views. The proximal end of the ilium is not preserved and part of the pubis is damaged. (k–l) Left astragalus (IPS56478t). (m–n) Left calcaneus (IPS56468s). fp, fibular process; st, sulcus tali; sup, sustentacular process. Scale bar is 2 cm in figures (a–j) and 1 cm in figures (k–n). For a reconstruction of the skeleton see Figure 1, Videos 1 and 3D model in Supplementary file 1. Details of particular bones are shown in Figure 5; Figure 2—figure supplement 1. For a detailed description and comparison of the postcranial bones of M. neogrivensis see Appendix 3.3. https://doi.org/10.7554/eLife.39270.004 Figure 3 Download asset Open asset Mandible and cheek teeth of Miopetaurista neogrivensis. (a to c) Partial left hemimandible (IPS56468j) in lateral, medial and dorsal views. (d to e) Partial right hemimandible (IPS56468i) in lateral and medial views. A caudal vertebra and a bone fragment are attached to the lateral side of the mandibular ramus. Both hemimandibles were associated to the partial skeleton IPS56468 from ACM/C5-D1. (f to g) Partial hemimandible (IPS87560) from ACM/C8-B sector in lateral and medial views. (h) Left upper cheek teeth series (P3–M3) of IPS56468h (Figure 6—Figure supplement 1 ). (i) Left lower cheek teeth series (p4–m3) of IPS56468j. Cheek teeth measurements are given in Supplementary file 4 whereas mandibular measurements are given in Supplementary file 6. For a detailed description and comparisons of cheek teeth and mandible morphology see Appendix 3.1 and 3.2. an, angular process; ar, articular process; co, coronoid process. Scale bar is 1 cm in figs. a to g; 2 mm in (h to i). https://doi.org/10.7554/eLife.39270.006 Figure 4 Download asset Open asset Carpal bones associated with the extension of the patagium of Miopetaurista neogrivensis as compared to extant squirrels. Articulated bones are shown on top and disarticulated ones are shown below. (a) Miopetaurista neogrivensis. (b) Petaurista petaurista, large-sized flying squirrel, subtribe Pteromyina. (c) Hylopetes sagitta, small-sized flying squirrel, subtribe Glaucomyina. (d) Sciurus vulgaris, tree squirrel, tribe Sciurini. The patagium is supported by the styliform cartilage which is attached to the pisiform bone. Flying squirrels present an elevated process for articulation with the scapholunate in the pisiform, whereas in tree squirrels this bone only articulates with the triquetrum and the ulna. In addition, note the presence of a triquetral process in Miopetaurista and Petaurista, characteristic of the Pteromyina. All extant specimens are kept in the collections of the Naturalis Biodiversity Center (Leiden, the Netherlands). See Video 2 for an animated version of this figure. Collection numbers of the scanned specimens and computed tomography parameters used are given in Table 5. Tridimensional models generated from µCT scan data. pi, pisiform (in blue); sl, scapholunate (in yellow); slp, scapholunate process of the pisiform; tr, triquetrum (in red); trp, triquetral processes of the pisiform; ulp, ulnar process of the pisiform. Scale bar is 1 cm. https://doi.org/10.7554/eLife.39270.007 Figure 5 with 1 supplement see all Download asset Open asset Comparison of the limb bones of extant ground, tree and flying squirrels with Miopetaurista neogrivensis. All elements are scaled to femur length and shown in anterior view. Humerus (a–e) and articulated femur and tibia (f–j) of: (a,f) the xerin ground squirrel Xerus erythropus; (b,g) the callosciurin tree squirrel Callosciurus prevostii; (c,h) the small-sized flying squirrel (subtribe Glaucomyina) Hylopetes sagitta; (d,i) the large-sized fying squirrel (subtribe Pteromyina) Petaurista petaurista; (e,j) Miopetaurista neogrivensis. Note that limb bones of flying squirrels and M. neogrivensis are much longer and more slender than those of tree and ground squirrels. Furthermore, processes and areas for the insertion of the main limb muscles are reduced. For a description and comparison of the postcranial bones of M. neogrivensis, see Appendix 3.3. See Supplementary file 7 for the collection numbers of the figured specimens and postcranial measurements. All bones are right elements, except for a–b and f–g, which are reversed left elements. Scale bar is 1 cm. https://doi.org/10.7554/eLife.39270.008 Table 1 Catalogue of bones and bone fragments composing the partial skeleton of Miopetaurista neogrivensis. This list includes the catalogue numbers (preceded by the acronym ‘IPS’) of the various bones and bone fragments belonging to the partial skeleton of a single individual of Miopetaurista neogrivensis (IPS56468) from locality ACM/C5-D1. IPS, acronym for the collections of the Institut Català de Paleontologia Miquel Crusafont. https://doi.org/10.7554/eLife.39270.010 Catalogue no.RegionDescriptionIPS56468alegright tibiaIPS56468blegright femurIPS56468clegleft femurIPS56468dlegdistal half of the left tibiaIPS56468earmleft humerusIPS56468farmright humerusIPS56468garmdistal half of the right radius, with damaged epiphysisIPS56468hcraniumalmost complete cranium, laterally compressed in an oblique angleIPS56468icranium + tailpartial right mandible (angular process broken), caudal vertebra (probably corresponding to the mid part of the tail)IPS56468jcraniumpartial left mandible (articular process broken, all other processes with minor damage)IPS56468kpelvic girdlepartial right coxal (proximal end of the ilium and part of the pubis damaged)IPS56468lpelvic girdlepartial left coxal (missing most of the pubis and ischium, extensive damage in the ilium)IPS56468mtrunklumbar vertebrae (L3–L4) in anatomical connectionIPS56468ntrunklumbar vertebrae (L5–L6) in anatomical connectionIPS56468oneckpartial axis (only part of the vertebral body is preserved) and partial cervical vertebra (C3)IPS56468ptrunkthoracic vertebra (T1?)IPS56468qtailfour caudal vertebrae (mid part of the tail) that articulate with one anotherIPS56468rtrunkseven rib fragmentsIPS56468sankleleft calcaneus and left navicularIPS56468tankleleft astragalusIPS56468utrunkthree partial thoracic vertebrae (T2–T4?) that articulate with one anotherIPS56468vindeterminateassociated bone fragments (may not belong to M. neogrivensis)IPS56468windeterminateassociated bone fragments (may not belong to M. neogrivensis)IPS56468xfoot?six distal phalanges which are not assigned to any particular ray or side; attribution to the foot is tentativeIPS56468ytrunktwo sternebrae that articulate with one anotherIPS56468zfootleft metatarsals 2–4 in anatomical connectionIPS56468aathoracic girdleright clavicle (with minor damage in its acromial end) and partial left clavicle (acromial end missing)IPS56468abfootcomplete right metatarsal 3, and partial rigth metatarsals 4 (proximal end missing), 2 and 4 (only distal half preserved)IPS56468acfootfour proximal phalanges and one partial proximal phalanx (distal half); they are not assigned to any particular ray or sideIPS56468adfoot?seven intermediate phalanges and five fragments; they are not assigned to any particular ray or side and attribution to the foot is tentativeIPS56468aehandfour proximal phalanges; they are not assigned to any particular ray or sideIPS56468afankleleft intermediate and medial cuneiformIPS56468agankleright navicularIPS56468ahwristright scapholunate and dorsal end of the right pisiform Table 2 Catalogue of additional material of Miopetaurista neogrivensis. This list includes the additional material of Miopetaurista neogrivensis from locality ACM/C5-D1 and the approximately stratigraphicaly equivalent localities ACM/C8-Af and ACM/C6-A5, as well as from sector ACM/C8-B. IPS, acronym for the collections of the Institut Català de Paleontologia Miquel Crusafont. https://doi.org/10.7554/eLife.39270.011 Catalogue no.LocalityAnatomical elementIPS43480ACM/C5-D1L m1IPS43505ACM/C5-D1L m3IPS43675ACM/C5-D1R P4IPS43677ACM/C5-D1partial left mandible with p4–m3 (only part of the mandibular body preserved)IPS43724ACM/C5-D1right maxillary fragment with partial P4-M2IPS77856ACM/C5-D1R P4IPS77857ACM/C5-D1R P4IPS77858ACM/C5-D1R M1/M2IPS77859ACM/C5-D1R M1/M2IPS77860ACM/C5-D1fragment of R M1/M2IPS77861ACM/C5-D1fragment of R M1/M2IPS77862ACM/C5-D1L M1/M2IPS77863ACM/C5-D1broken L M1/M2IPS77864ACM/C5-D1fragment of L M1/M2IPS77865ACM/C5-D1fragment of L M1/M2IPS77866ACM/C5-D1L M3IPS77867ACM/C5-D1R M3IPS77868ACM/C5-D1L dp4IPS77869ACM/C5-D1fragment of L dp4IPS77870ACM/C5-D1R dp4IPS77871ACM/C5-D1L p4IPS77872ACM/C5-D1R p4IPS77873ACM/C5-D1R p4IPS77874ACM/C5-D1L m1IPS77875ACM/C5-D1L m1IPS77876ACM/C5-D1L m1IPS77877ACM/C5-D1L m2IPS77878ACM/C5-D1L m2IPS77879ACM/C5-D1broken L m1/m2IPS77880ACM/C5-D1abraded L m1/m2IPS77881ACM/C5-D1fragment of L m1/m2IPS77882ACM/C5-D1fragment of L m1/m2IPS77883ACM/C5-D1R m1IPS77884ACM/C5-D1lingually abraded R m1IPS77885ACM/C5-D1broken R m1/m2IPS77886ACM/C5-D1R m3IPS77887ACM/C5-D1fragment of upper molarIPS77888ACM/C5-D1fragment of lower molarIPS78179ACM/C5-D1L M1/M2IPS85340ACM/C5-D1fragment of left mandible with m1–m3 and associated p4IPS85410ACM/C6-A5partial cranium (includes the dorsal half of the skull as well as part of the right zygomatic arch and maxillary bone with damaged P4–M3)IPS87560ACM/C8-B sectorpartial left mandible with p4–m3 (incisor and coronoid process broken, p4 damaged)IPS88677ACM/C8-Afpartial cranium (dorsoventrally crushed) Video 1 Download asset This video cannot be played in place because your browser does support HTML5 video. You may still download the video for offline viewing. Download as MPEG-4 Download as WebM Download as Ogg Reconstruction of the skeleton and life appearance of Miopetaurista neogrivensis. The squirrel is shown reducing speed just before landing on a tree branch. Skeleton reconstruction based in the partial skeleton IPS56468 from Abocador de Can Mata. Coat pattern and color are based in extant Petaurista species, the sister taxon of Miopetaurista. A high-quality 3D surface model of the reconstructed skeleton is available at MorphoBank https://morphobank.org/index.php/Projects/ProjectOverview/project_id/3108 https://doi.org/10.7554/eLife.39270.012 Extant and fossil flying squirrels have been classified into different groups according to the complexity of dental morphology (Mein, 1970). The cheek teeth of Miopetaurista show a simple occlusal pattern, with enamel wrinkling only in the lower molars and no additional lophules (Figure 3, Appendix 3.1). This pattern clearly differs from the more complex one of other large-sized flying squirrels, such as Aeretes and Petaurista (Mein, 1970; Thorington et al., 2002). Therefore, Miopetaurista has been included within the group that comprises Aeromys and the small-sized flying squirrels, which do show simple dental patterns (Mein, 1970). However, our phylogenetic analyses (see below) show that M. neogrivensis is the sister taxon of extant Petaurista, a genus that would belong to a completely different group according to dental classification (Mein, 1970). Considering dental morphology Petaurista is assigned to a group characterized by its complex dental pattern with additional transverse lophules which would also comprise the genera Aeretes, Belomys, Eupetaurus and Trogopterus, among others (Mein, 1970). This clearly illustrates that dental characters, although useful to diagnose the different species and genera, should not warrant high consideration for disentangling the phylogenetic relationships between flying squirrels. Morphological description and comparisons Among the recovered postcranial material, a complete scapholunate and the dorsal end of the pisiform (Figure 4 and Video 2) are the most diagnostic elements of pteromyins, because they form the functional complex associated with the extension of the gliding membrane (Thorington, 1984; Thorington et al., 2005; Thorington et al., 2002; Thorington and Darrow, 2000). The styliform cartilage, which supports the patagium in all members of the group, attaches to the pisiform and is extended when the wrist is radially abducted and dorsiflexed (Thorington, 1984; Thorington and Darrow, 2000). The pisiform of M. neogrivensis displays an elevated process for the articulation with the scapholunate (Figure 4 and Video 2). This is characteristic of pteromyins, serving as a stabilizer of the styliform cartilage, whereas in other squirrels this bone articulates only with the triquetrum and the distal end of the ulna. Moreover, in the scapholunate of M. neogrivensis, the articular surface for the radius is much more convex than in tree squirrels, thus resembling the flying squirrel condition, which enables a greater radial abduction. Therefore, the proximal wrist joint morphology of M. neogrivensis indicates that this species belongs to the pteromyin clade and provides the oldest evidence of gliding locomotion in sciurids (see also Appendix 3.3). The latter is further confirmed by other postcranial adaptations shared with extant pteromyins (Thorington et al., 2005), including the elongated and slender limb bones with reduced muscular attachments (Figure 5 and Figure 5—figure supplement 1), which enhance joint extension during gliding (Thorington et al., 2005), as well as the elongated lumbar vertebrae (Figure 2; see Appendix 3.3 for a detailed description and comparisons of the postcranial elements). The elongation of lumbar vertebrae and limbs determines the size and shape of the patagium and dictates important aerodynamic features, such as the decreased wing loading of flying squirrels (Thorington and Heaney, 1981; Thorington and Santana, 2007). Video 2 Download asset This video cannot be played in place because your browser does support HTML5 video. You may still download the video for offline viewing. Download as MPEG-4 Download as WebM Download as Ogg Proximal carpal bones of Miopetaurista neogrivensis as compared to tree and flying squirrels. Miopetaurista neogrivensis is compared to Petaurista petaurista (large-sized flying squirrel; subtribe Pteromyina); Hylopetes sagitta (small-sized flying squirrel; subtribe Glaucomyina); and Sciurus vulgaris (tree squirrel; tribe Sciurini). These bones form the morphofunctional complex associated with extension of the patagium. The flying membrane is supported by the styliform cartilage which is attached to the pisiform bone. High-quality 3D surface models of the carpal bones of Miopeataurista and other squirrels are available at MorphoBank https://morphobank.org/index.php/Projects/ProjectOverview/project_id/3108 https://doi.org/10.7554/eLife.39270.013 Based on morphological (Thorington et al., 2002) and molecular data (Mercer and Roth, 2003), flying squirrels are divided into two distinct subtribes: Pteromyina, comprising large-sized forms, and Glaucomyina, for the small-sized ones (Thorington and Hoffmann, 2005). The skeleton of M. neogrivensis morphologically resembles that of the Pteromyina, further being comparable in size to their largest representatives. Body mass was estimated by means of an allometric regression of body mass vs. skull length in extant sciurids (see Materials and Methods), resulting in 1339 g (50% confidence intervals 1116 – 1606 g thus being in the range of most species of the extant giant flying squirrel Petaurista (about 1200 – 2000 g; Thorington et al., 2012). The long bones are almost indistinguishable of Petaurista. The skull, which was virtually reconstructed from two well-preserved specimens (Figure 6, Figure 6—figure supplement 1-2, Video 3, Table 3), is strikingly similar in size and morphology to that of the other large-sized flying squirrels, particularly Aeromys and Petaurista (for a detailed morphological description of the skull and comparisons see Appendix 3.2). These genera are characterized by their short and wide rostrum, moderately inflated bullae and relatively wide posterior region of the skull. Other morphological similarities include the robust and long postorbital process that partially encloses the orbit, the well-developed jugal process in the zygomatic arch and the presence of two septa in the tympanic cavity (Video 4; Appendix 3.2). Most of the smaller flying squirrels show more elongate muzzles, slender or shorter postorbital processes and, in some cases, a higher number of transbullar septa. The proximal carpal bones of M. neogrivensis not only unambiguously indicate that it is a flying squirrel, but also allow assigning it to the Pteromyina (Figure 4 and Video 2). The pisiform displays a distinct spur (triquetral process) that fits between the palmar surfaces of the scapholunate and the triquetrum. This process is completely lacking in the Glaucomyina (Thorington et al., 2002; Thorington and Darrow, 2000) (Figure 4 and Video 2; see also Appendix 3.3). Both subtribes are also distinguished by the origin of the tibiocarpalis muscle, which runs from the ankle to the tip of the styliform cartilage, defining the edge of the patagium. In the Glaucomyina the tibiocarpalis originates from a tuberosity on the distal tibia which is lacking in M. neogrivensis and the Pteromyina (Thorington et al., 2002). In the latter, the tibiocarpalis originates from the metatarsals instead. Figure 6 with 2 supplements see all Download asset Open asset Reconstruction of the cranium of Miopetaurista neogrivensis. Virtual reconstruction based on µCT scan data from specimens IPS56468h (see Figure 6—figure supplement 1) and IPS88677 (see Figure 6—figure supplement 2). Specimen IPS56468h was used as the basis for the reconstruction, with missing elements taken from IPS88677 (Table 3. (a) Dorsal view. (b) Ventral view. (c) Lateral (left) view. (d) Anterior view. (e) Lateral (right) view. (f) Posterior view. See Video 3 for an animated version of the skull reconstruction. For a detailed description of skull morphology see Appendix 3.2. Cranial measurements for original fossil specimens (IPS56468h, IPS88677) as well as for the virtually reconstructed cranium are given in Supplementary file 5. ab, auditory bulla; am, auditory meatus; as, alisphenoid; bo, basioccipital; fm, foramen magnum; fr, frontal; if, incisive foramen; ifo, infraorbital foramen; ju, jugal; msp, mastoid process; mt, masset
In the last decade, the first ichnoassamblages from the middle Muschelkalk facies (upper Anisian–middle Ladinian) of the Catalan Basin (NE Iberian Peninsula) have been discovered. Herein, the first xiphosuran trace fossils are described from the locality of Penya Rubí, a newly discovered ichnosite from the Catalan Basin. The finding opens a window into peri-Tethys ecosystems with coastal influence. The traceway is referred to the ichnogenus Kouphichnium, a locomotion trace attributed to xiphosurans. The traceway preserves telson grooves and different imprint morphologies from the various appendages. The traceway pattern and arrangement of the different traces suggest a crawling locomotion style. The sedimentology suggests a coastal zone with areas influenced by tides (intertidal flat). The morphological variations of the ichnites are correlated to substrate rheology, the locomotion of the tracemaker and environmental conditions.
Finite Element Analysis (FEA) is a useful method for understanding form and function.However, modelling of fossil taxa invariably involves assumptions as a result of preservation-induced loss of information in the fossil record.To test the validity of predictions from FEA, given such assumptions, these results could be compared to independent lines of evidence for cranial mechanics.In the present study a new concept of using bone microstructure to predict stress distribution in the skull during feeding is put forward and a correlation between bone microstructure and results of computational biomechanics (FEA) is carried out.The bony framework is a product of biological optimisation; bone structure is created to meet local mechanical conditions.To test how well results from FEA correlate to cranial mechanics predicted from bone structure, the well-known temnospondyl Metoposaurus krasiejowensis was used as a model.A crucial issue to Temnospondyli is their feeding mode; did they suction feed or employ direct biting, or both?Metoposaurids have previously been characterised either as active hunters or passive bottom dwellers.In order to test the correlation between results from FEA and bone microstructure, two skulls of Metoposaurus were used, one modelled under FE analyses, while for the second one 17 dermal bone microstructure were analysed.Thus, for the first time, results predicting cranial mechanical behaviour using both methods are merged to understand the feeding strategy of Metoposaurus.Metoposaurus appears to have been an aquatic animal that exhibited a generalist feeding behaviour.This taxon may have used two foraging techniques in hunting; mainly bilateral biting and, to a lesser extent, lateral strikes.However, bone microstructure suggests that lateral biting was more
Background Megaloolithid eggs have long been associated with sauropod dinosaurs. Despite their extensive and worldwide fossil record, interpretations of egg size and shape, clutch morphology, and incubation strategy vary. The Pinyes locality in the Upper Cretaceous Tremp Formation in the southern Pyrenees, Catalonia provides new information for addressing these issues. Nine horizons containing Megaloolithus siruguei clutches are exposed near the village of Coll de Nargó. Tectonic deformation in the study area strongly influenced egg size and shape, which could potentially lead to misinterpretation of reproductive biology if 2D and 3D maps are not corrected for bed dip that results from tectonism. Methodology/Findings Detailed taphonomic study and three-dimensional modelling of fossil eggs show that intact M. siruguei clutches contained 20–28 eggs, which is substantially larger than commonly reported from Europe and India. Linear and grouped eggs occur in three superimposed levels and form an asymmetric, elongate, bowl-shaped profile in lateral view. Computed tomography data support previous interpretations that the eggs hatched within the substrate. Megaloolithid clutch sizes reported from other European and Indian localities are typically less than 15 eggs; however, these clutches often include linear or grouped eggs that resemble those of the larger Pinyes clutches and may reflect preservation of incomplete clutches. Conclusions/Significance We propose that 25 eggs represent a typical megaloolithid clutch size and smaller egg clusters that display linear or grouped egg arrangements reported at Pinyes and other localities may represent eroded remnants of larger clutches. The similarity of megaloolithid clutch morphology from localities worldwide strongly suggests common reproductive behaviour. The distinct clutch geometry at Pinyes and other localities likely resulted from the asymmetrical, inclined, and laterally compressed titanosaur pes unguals of the female, using the hind foot for scratch-digging during nest excavation.
The great ape and human clade (Primates: Hominidae) currently includes orangutans, gorillas, chimpanzees, bonobos, and humans. When, where, and from which taxon hominids evolved are among the most exciting questions yet to be resolved. Within the Afropithecidae, the Kenyapithecinae (Kenyapithecini + Equatorini) have been proposed as the sister taxon of hominids, but thus far the fragmentary and scarce Middle Miocene fossil record has hampered testing this hypothesis. Here we describe a male partial face with mandible of a previously undescribed fossil hominid, Anoiapithecus brevirostris gen. et sp. nov., from the Middle Miocene (11.9 Ma) of Spain, which enables testing this hypothesis. Morphological and geometric morphometrics analyses of this material show a unique facial pattern for hominoids. This taxon combines autapomorphic features--such as a strongly reduced facial prognathism--with kenyapithecine (more specifically, kenyapithecin) and hominid synapomorphies. This combination supports a sister-group relationship between kenyapithecins (Griphopithecus + Kenyapithecus) and hominids. The presence of both groups in Eurasia during the Middle Miocene and the retention in kenyapithecins of a primitive hominoid postcranial body plan support a Eurasian origin of the Hominidae. Alternatively, the two extant hominid clades (Homininae and Ponginae) might have independently evolved in Africa and Eurasia from an ancestral, Middle Miocene stock, so that the supposed crown-hominid synapomorphies might be homoplastic.
Temnospondyls from the Middle–Late Triassic of Madagascar are problematic and scarce: ‘Metoposaurus hoffmani’ was erected on the basis of poor material, and this taxon has never been revised. Other remains were also reported and assigned to Temnospondyli indet., but they have never been described, nor figured. Here, we (re)describe in detail this historical material from the Folakara area of Madagascar (Isalo Group, Morondava Basin): the specimens include cranial and postcranial remains, most of them being referred to Metoposauridae indet. and a few to Stereospondyli indet. We also confirm that ‘M. hoffmani’ is a nomen dubium owing to the absence of any clear autapomorphy of the fragmentary type material. The material referred here to Metoposauridae indet. is incorporated in an updated paleobiogeographic analysis of the group: interestingly, it suggests a connection with Indian metoposaurids during the Late Triassic.
Biting is an integral feature of the feeding mechanism for aquatic and terrestrial salamanders to capture, fix or immobilize elusive or struggling prey. However, little information is available on how it works and the functional implications of this biting system in amphibians although such approaches might be essential to understand feeding systems performed by early tetrapods. Herein, the skull biomechanics of the Chinese giant salamander, Andrias davidianus is investigated using 3D finite element analysis. The results reveal that the prey contact position is crucial for the structural performance of the skull, which is probably related to the lack of a bony bridge between the posterior end of the maxilla and the anterior quadrato-squamosal region. Giant salamanders perform asymmetrical strikes. These strikes are unusual and specialized behavior but might indeed be beneficial in such sit-and-wait or ambush-predators to capture laterally approaching prey. However, once captured by an asymmetrical strike, large, elusive and struggling prey have to be brought to the anterior jaw region to be subdued by a strong bite. Given their basal position within extant salamanders and their "conservative" morphology, cryptobranchids may be useful models to reconstruct the feeding ecology and biomechanics of different members of early tetrapods and amphibians, with similar osteological and myological constraints.
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