The Late Cretaceous eutherian Zalambdalestes reveals unique axis and complex evolution of the mammalian neck.

The typical mammalian neck consisting of seven cervical vertebrae (C1-C7) was established by the Late Permian in the cynodont forerunners of modern mammals. This structure is precisely adapted to facilitate movements of the head during feeding, locomotion, predator evasion, and social interactions. Eutheria, the clade including crown placentals, has a fossil record extending back more than 125 million years revealing significant morphological diversification in the Mesozoic. Yet very little is known concerning the early evolution of eutherian cervical morphology and its functional adaptations. A specimen of Zalambdalestes lechei from the Late Cretaceous of Mongolia boasts exceptional preservation of an almost complete series of cervical vertebrae (C2-C7) revealing a highly modified axis (C2). The significance of this cervical morphology is explored utilizing an integrated approach combining comparative anatomical examination across mammals, muscle reconstruction, geometric morphometrics and virtual range of motion analysis. We compared the shape of the axis in Zalambdalestes to a dataset of 88 mammalian species (monotremes, marsupials, and placentals) using three-dimensional landmark analysis. The results indicate that the unique axis morphology of Zalambdalestes has no close analog among living mammals. Virtual range of motion analysis of the neck strongly implies Zalambdalestes was capable of exerting very forceful head movements and had a high degree of ventral flexion for an animal its size. These findings reveal unexpected complexity in the early evolution of the eutherian cervical morphology and suggest a feeding behavior similar to insectivores specialized in vermivory and defensive behaviors in Zalambdalestes akin to modern spiniferous mammals.

The first complete mitochondrial genome data of the Afghan pika Ochotona rufescens (Lagomorpha, Ochotonidae), near the type locality.

The Afghan pika Ochotona rufescens (Gray, 1842) is widely distributed across the mountains of Afghanistan, Iran, Pakistan, and southwestern Turkmenistan, most often at elevations between 2,000 and 3,000 m. Here we present, for the first time, the complete mitochondrial genomes of two specimens of the nominotypical subspecies Ochotona rufescens rufescens, de novo assembled from Illumina short reads of fragmented probe-enriched DNA. The lengths of the circular mitogenomes are 16,408 bp and 16,407 bp, respectively. Both mitogenomes contain 13 protein-coding genes (PCGs), two ribosomal RNAs (16S rRNA and 12S rRNA), 22 transfer RNA genes, and a control region. The gene NAD6 and the tRNA (Gln), tRNA (Ala), tRNA (Asn), tRNA (Cys), tRNA (Tyr), tRNA (Ser), tRNA (Glu), and tRNA (Pro) are encoded on the light strand while the rest are encoded on the heavy strand. The overall nucleotide composition was ∼30% for A, 25% for T, 15% for G, and 29% for C. The mitogenome data are available in the GenBank under the accession numbers ON859136 and ON859137.

The mammalian skull: development, structure and function.

The mammalian skull is an informative and versatile study system critical to research efforts across the broad spectrum of molecular, cellular, organismal and evolutionary sciences. The amount of knowledge concerning mammalian skull continues to grow exponentially, fuelled by the advent of new research methods and new material. Computed microtomography, including X-ray imaging using synchrotron radiation, proved to be an important tool for the descriptive and quantitative analysis of cranial anatomy. A major conceptual change, namely combining genetics and development with evolution into 'evo-devo' studies, also contributed to our knowledge of the mammalian skull enormously. These advances, coupled with novel techniques now allow researchers to integrate the process of cranial development with data from the fossil record, which is also augmented by seminal discoveries from Africa, Asia and both Americas. However, for decades, there has been no comprehensive source covering fundamental aspects of this vibrant field of evolutionary biology. To address this gap, we offer in this theme issue a balanced mix of research papers and reviews from leading experts in the field and a younger generation of scientists from five continents. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

Auditory region circulation in Lagomorpha: the internal carotid artery pattern revisited.

The internal carotid artery (ICA) is one of the major vessels in the cranial circulation. Characters concerning the ICA, such as its course in the auditory region, have been employed frequently in phylogenetic analyses of mammals, including extinct taxa. In lagomorphs, however, our knowledge on vascular features of the auditory region has been based predominantly on living species, mostly on the European rabbit. We present the first survey on 11 out of 12 extant genera and key fossil taxa such as stem lagomorphs and early crown representatives (Archaeolagus and Prolagus). The ICA pattern shows a modified transpromontorial course in stem taxa (Litolagus, Megalagus and Palaeolagus) and Archaeolagus, which we propose as the ancestral character state for Lagomorpha, similar to that for the earliest rodents, plesiadapids and scandentians. The ICA pattern in leporids is perbullar, but shows structural similarities to stem taxa, whereas the extrabullar ICA course in Ochotona is apparently a highly derived condition. Prolagus shows a mixed character state between leporids and Ochotona in its ICA route. The persistence of the transpromontorial ICA course and similarities in the carotid canal structure among stem taxa and crown leporids support morphological conservatism in Lagomorpha, in contrast to their sister clade Rodentia. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

Mandibular characteristics of early Glires (Mammalia) reveal mixed rodent and lagomorph morphotypes.

Glires (rodents, lagomorphs and their fossil kin) is the most speciose and arguably most diversified clade of living placentals. Different lineages within the Glires evolved basically opposite chewing movements: a mostly transversal power stroke in lagomorphs, and a mostly proal power stroke in rodents, but the ancestral condition for Glires is still unclear. To address this knowledge gap, we studied the mandibles of Chinese Palaeocene Glires representing the duplicidentate (lagomorph-like; Mimotona) and simplicidentate (rodent-like; Eomylus and Heomys) lineages. To assess the mechanical resistance of mandibles to bending and torsion, we calculated the section modulus. The dentaries differ greatly in morphology and the region where the maximum grinding force was likely applied. The early Palaeocene Mimotona lii and the middle Palaeocene Mimotona robusta and Heomys orientalis all show a pattern of increasing strength moving posteriorly along the mandible, similar to sciurids and the mountain beaver. By contrast, the late Palaeocene Eomylus sp. mandible was strongest in the m1 region, a pattern seen in lagomorphs and the stem placental Zofialestes. Our results indicate the early diversification of mandible structure of Glires, demonstrate a mixture of duplicidentate and simplicidentate characters among the basal Glires and suggest an early occurrence of a lagomorph-like morphotype. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

Locomotor behavior and hearing sensitivity in an early lagomorph reconstructed from the bony labyrinth.

The structure of the bony labyrinth is highly informative with respect to locomotor agility (semicircular canals [SCC]) and hearing sensitivity (cochlear and oval windows). Here, we reconstructed the agility and hearing sensitivity of the stem lagomorph Megalagus turgidus from the early Oligocene of the Brule Formation of Nebraska (USA). Megalagus has proportionally smaller SCCs with respect to its body mass compared with most extant leporids but within the modern range of variability, suggesting that it was less agile than most of its modern relatives. A level of agility for Megalagus within the range of modern rabbits is consistent with the evidence from postcranial elements. The hearing sensitivity for Megalagus is in the range of extant lagomorphs for both low- and high-frequency sounds. Our data show that by the early Oligocene stem lagomorphs had already attained fundamentally rabbit-like hearing sensitivity and locomotor behavior, even though Megalagus was not a particularly agile lagomorph. This is likely because Megalagus was more of a woodland dweller than an open-habitat runner. The study of sensory evolution in Lagomorpha is practically unknown, and these results provide first advances in understanding the primitive stages for the order and how the earliest members of this clade perceived their environment.

The first complete mitochondrial genome data of the pygmy rabbit Brachylagus idahoensis, the world's smallest leporid.

The pygmy rabbit Brachylagus idahoensis (Merriam, 1891) is the smallest extant leporid, which naturally occurs in the Great Basin and adjacent areas in western parts of the United States of America. Its distribution is strongly associated with the sagebrush (Artemisia ssp.) vegetation. Here we present, for the first time, the complete mitochondrial genome of Brachylagus idahoensis, de novo assembled from Illumina short reads of fragmented probe-enriched DNA. The circular mitogenome is 17,021 bp in length and contains 13 protein-coding genes (PCGs), two ribosomal RNAs (16S rRNA and 12S rRNA), 22 transfer RNA genes, and a control region. The gene NAD6 and the tRNA(Gln), tRNA(Ala), tRNA(Asn), tRNA(Cys), tRNA(Tyr), tRNA(Ser), tRNA(Glu) and tRNA(Pro) are encoded on the light strand while the rest are encoded on the heavy strand. The overall nucleotide composition was 30.78% for A, 28.5% for T, 13.62% for G and 27.08% for C. The mitogenome data are available in the GenBank under the accession number OL436257.

Tarsal morphology of ischyromyid rodents from the middle Eocene of China gives an insight into the group's diversity in Central Asia.

Ischyromyids are a group of large rodents with the earliest fossil record known from the late Paleocene (Clarkforkian) of North America; they are considered the earliest fossil representatives of Rodentia of modern aspect. Ischyromyids dominated early Paleogene small-mammal assemblages of North America and in the latest Paleocene migrated to western Europe and to Asia; in the latter they survived only to the beginning of the late Eocene, but were never abundant. Here we describe for the first time the calcanei of ischyromyids from the early middle Eocene of the Erlian Basin in Nei Mongol, northern China. These calcanei document the existence of three species. The morphology of the studied tarsal bones overall suggests ambulatory locomotion for these animals ('slow cursors'), similar to that of the coypu and porcupines, but one form shows more marked cursorial capabilities. These differences show that Chinese ischyromyids, although rare, had attained greater taxonomic diversity by the middle Eocene in Nei Mongol than estimated from dental remains. We also address the question of the morphological and ecological divergence of these ischyromyids in relation to their North American counterparts, as well as the issue of a direct dispersal route from North America to Asia in the early Eocene.

Cranial endocast of the stem lagomorph Megalagus and brain structure of basal Euarchontoglires.

Early lagomorphs are central to our understanding of how the brain evolved in Glires (rodents, lagomorphs and their kin) from basal members of Euarchontoglires (Glires + Euarchonta, the latter grouping primates, treeshrews, and colugos). Here, we report the first virtual endocast of the fossil lagomorph Megalagus turgidus, from the Orella Member of the Brule Formation, early Oligocene, Nebraska, USA. The specimen represents one of the oldest nearly complete lagomorph skulls known. Primitive aspects of the endocranial morphology in Megalagus include large olfactory bulbs, exposure of the midbrain, a small neocortex and a relatively low encephalization quotient. Overall, this suggests a brain morphology closer to that of other basal members of Euarchontoglires (e.g. plesiadapiforms and ischyromyid rodents) than to that of living lagomorphs. However, the well-developed petrosal lobules in Megalagus, comparable to the condition in modern lagomorphs, suggest early specialization in that order for the stabilization of eye movements necessary for accurate visual tracking. Our study sheds new light on the reconstructed morphology of the ancestral brain in Euarchontoglires and fills a critical gap in the understanding of palaeoneuroanatomy of this major group of placental mammals.

Appendicular skeleton of Protoceratops andrewsi (Dinosauria, Ornithischia): comparative morphology, ontogenetic changes, and the implications for non-ceratopsid ceratopsian locomotion.

Protoceratops andrewsi is a well-known ceratopsian dinosaur from the Djadokhta Formation (Upper Cretaceous, Mongolia). Since the 1920s, numerous skeletons of different ontogenetic stages from hatchlings to adults, including fully articulated specimens, have been discovered, but the postcranial anatomy of Protoceratops has not been studied in detail. A new, mostly articulated subadult individual provides an excellent opportunity for us to comprehensively describe the anatomy of the limb skeleton, to compare to other ceratopsian dinosaurs, and to study the ontogenetic and intraspecific variation in this species. New data provided by the specimen shed light on the lifestyle of P. andrewsi. The young subadult individuals present an array of morphological characters intermediate between the bipedal Psittacosaurus and fully quadrupedal adult P. andrewsi. We compare these observations with a broad range of non-ceratopsid Neoceratopsia (of various locomotor adaptations) and Psittacosauridae (obligate bipeds), which gives us insight into the evolution of the skeletal characters informative for the postural change in ceratopsian dinosaurs.

Oldest ctenodactyloid tarsals from the Eocene of China and evolution of locomotor adaptations in early rodents.

BACKGROUND: Tamquammys has been considered one of the basal ctenodactyloid rodents, which has been documented in the earliest to middle Eocene (~ 56.0-48.5 Ma) in China. It was the most abundant and widespread rodent genus in the Erlian Basin (Nei Mongol, China) and dominated Arshantan small-mammal faunas of that region. Here for the first time we describe the morphology of the astragalocalcaneal complex in Tamquammys robustus (larger) and T. wilsoni, and interpret it against the background of locomotor adaptations of basal Euarchontoglires (rodents, lagomorphs, tree shrews, and primates). RESULTS: The comparative morphology of the tarsal elements in Tamquammys robustus and T. wilsoni shows overall slenderness of the bones and their similarity to the tarsal elements of Rattus, a generalist species, and those of small rock squirrels (e.g. Sciurotamias). The two species differ slightly in their cursorial ability; smaller T. wilsoni shows some adaptations to climbing. The results of principal component analysis of the calcaneus and astragalus support this observation and place T. robustus in-between Rattus and ground/rock squirrel morphospace, and T. wilsoni closer to euarchontans, Tupaia and Purgatorius. CONCLUSIONS: The morphology of the tarsal elements in Tamquammys indicates a generalist rodent morphotype with no particular adaptations to arboreality. We suggest that Tamquammys as a basal ctenodactyloid is closer to the ancestral astragalocalcaneal morphology of rodents than that of more derived North American paramyines of similar age. Overall similarity in Tamquammys tarsal elements structure to Purgatorius, a basal primate, may point to the antiquity of the tarsal structure in Tamquammys and a generally unspecialized foot structure in early Euarchontoglires.

A new Eocene anagalid (Mammalia: Euarchontoglires) from Mongolia and its implications for the group's phylogeny and dispersal.

Anagalidae are extinct primitive Euarchontoglires from Asia, regarded as relatively closely related to basal Glires. So far, the group has been reported only from China and stratigraphically spans from the early Paleocene to the latest Eocene/earliest Oligocene. Anagalids are characterized by a relatively full dental formula featuring slightly enlarged semi-procumbent incisors, prominent canines, and tall cheek teeth with usually heavily worn crowns, indicative of an abrasive diet. Here we report a new genus and species from the late Eocene Ergilin Dzo Formation in southern Mongolia. The first non-Chinese anagalid is also the northernmost record of the family. Zofiagale ergilinensis gen. and sp.nov. is remarkable for its relatively small size (comparable only to the Paleocene genera Huaiyangale and Stenanagale), lack of P1, and molariform teeth showing almost no wear, suggesting a different diet than most Anagalidae. Furthermore, its molars display a strong buccal cingulum, a character in anagalids shared only with Wanogale. Our phylogenetic analysis of representatives of all anagalid genera based on 82 dental characters places Anagale and Anaptogale as the most basal lineages and clusters Zofiagale gen. nov. together with Qipania and Hsiuannania. These results suggest three independent northward dispersal events within the family in the late Eocene.

A large mimotonid from the middle Eocene of China sheds light on the evolution of lagomorphs and their kin.

Mimotonids share their closest affinity with lagomorphs and were a rare and endemic faunal element of Paleogene mammal assemblages of central Asia. Here we describe a new species, Mimolagus aurorae from the Middle Eocene of Nei Mongol (China). This species belongs to one of the most enigmatic genera of fossil Glires, previously known only from the type and only specimen from the early Oligocene of Gansu (China). Our finding extends the earliest occurrence of the genus by at least 10 million years in the Paleogene of Asia, which closes the gap between Mimolagus and other mimotonids that are known thus far from middle Eocene or older deposits. The new species is one of the largest known pre-Oligocene Glires. As regards duplicidentates, Mimolagus is comparable with the largest Neogene continental leporids, namely hares of the genus Lepus. Our results suggest that ecomorphology of this species was convergent on that of small perissodactyls that dominated faunas of the Mongolian Plateau in the Eocene, and probably a result of competitive pressure from other Glires, including a co-occurring mimotonid, Gomphos.

Comparative morphology of premolar foramen in lagomorphs (Mammalia: Glires) and its functional and phylogenetic implications.

Lagomorphs (a group that consists of pikas, hares, rabbits and allies) are notable for their conservative morphology retained for most of their over 50 million years evolutionary history. On the other hand, their remarkable morphological uniformity partly stems from a considerable number of homoplasies in cranial and dental structures that hamper phylogenetic analyses. The premolar foramen, an opening in the palate of lagomorphs, has been characterized as an important synapomorphy of one clade, Ochotonidae (pikas). Within Lagomorpha, however, its phylogenetic distribution is much wider, the foramen being present not only in all ochotonids but also in leporids and stem taxa; its morphology and incidence also varies considerably across the order, even intraspecifically. In this study, we provide a broad survey of the taxonomic distribution of the premolar foramen in extant and fossil Lagomorpha and describe in detail the morphological variation of this character within the group. Micro-computed tomography was used to examine the hard palate and infraorbital groove morphology in Poelagus (Leporidae) and Ochotona. Scans revealed the course and contacts of the canal behind the premolar foramen and structural differences between the two crown clades. We propose that the premolar foramen has evolved independently in several lineages of Lagomorpha, and we discuss development and function of this foramen in the lagomorph skull. This study shows the importance of comprehensive studies on phylogenetically informative non-dental characters in Lagomorpha.

The earliest occurrence of the steppe pika (Ochotona pusilla) in Europe near the Pliocene/Pleistocene boundary.

The steppe pika (Ochotona pusilla), a representative of the lagomorph family Ochotonidae, is restricted today to Kazakhstan and Russia. This subspecies-rich form belongs to a morphologically distinct, monospecific group of relatively small pikas, inhabiting steppe-like habitat. In the fossil record, it serves as a bioindicator of dry, grassland environment. The steppe pika was abundant and widespread in Europe during the Last Glaciation, and its unquestionable presence has been reported there since the middle Pleistocene. A new discovery of O. pusilla, from the Kielniki 3B locality (Poland), dated to the latest Pliocene, moves back the species appearance in Europe about one million years, almost coeval with its first record from the late Pliocene of Kazakhstan. Presence of such a typical steppe inhabitant as O. pusilla indicates significant climate change towards more arid, continental conditions, which started influencing Europe at 2.6 Ma. We present the first reliable record of the earliest O. pusilla entry deep into Europe in the latest Pliocene.