Hidden species diversity in an iconic living fossil vertebrate.

Ancient, species-poor lineages persistently occur across the Tree of life. These lineages are likely to contain unrecognized species diversity masked by the low rates of morphological evolution that characterize living fossils. Halecomorphi is a lineage of ray-finned fishes that diverged from its closest relatives before 200 Ma and is represented by only one living species in eastern North America, the bowfin, Amia calva Linnaeus. Here, we use double digest restriction-site-associated DNA sequencing and morphology to illuminate recent speciation in bowfins. Our results support the delimitation of a second living species of Amia, with the timing of diversification dating to the Plio-Pleistocene. This delimitation expands the species diversity of an ancient lineage that is integral to studies of vertebrate genomics and development, yet is facing growing conservation threats driven by the caviar fishery.

Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy.

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous3-17. Here we show that this key evolutionary transition can be investigated using the morphology of the endolymph-filled semicircular ducts of the inner ear, which monitor head rotations and are essential for motor coordination, navigation and spatial awareness18-22. Increased body temperatures during the ectotherm-endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics23,24, while simultaneously increasing behavioural activity25,26 probably required improved performance27. Morphological changes to the membranous ducts and enclosing bony canals would have been necessary to maintain optimal functionality during this transition. To track these morphofunctional changes in 56 extinct synapsid species, we developed the thermo-motility index, a proxy based on bony canal morphology. The results suggest that endothermy evolved abruptly during the Late Triassic period in Mammaliamorpha, correlated with a sharp increase in body temperature (5-9 °C) and an expansion of aerobic and anaerobic capacities. Contrary to previous suggestions3-14, all stem mammaliamorphs were most probably ectotherms. Endothermy, as a crucial physiological characteristic, joins other distinctive mammalian features that arose during this period of climatic instability28.

Response to Comment on "The early origin of a birdlike inner ear and the evolution of dinosaurian movement and vocalization".

David et al. claim that vestibular shape does not reflect function and that we did not use phylogenetic inference methods in our primary analyses. We show that their claims are countered by comparative and direct experimental evidence from across Vertebrata and that their models are empirically unverified. We did use phylogenetic methods to test our hypotheses. Moreover, their phylogenetic correction attempts are methodologically inappropriate.

Combined data analysis of fossil and living mammals: a Paleogene sister taxon of Placentalia and the antiquity of Marsupialia.

The Cretaceous-Paleogene (KPg) boundary, one of Earth's five major extinction events, occurred just before the appearance of Placentalia in the fossil record. The Gobi Desert, Mongolia and the Western Interior of North America have important fossil mammals occurring just before and after the KPg boundary (e.g. Prodiacodon, Deltatheridium) that have yet to be phylogenetically tested in a character-rich context with molecular data. We present here phylogenetic analyses of >6000 newly scored anatomical observations drawn from six untested fossils and added to the largest existing morphological matrix for mammals. These data are combined with sequence data from 27 nuclear genes. Results show the existence of a new eutherian sister clade to Placentalia, which we name and characterize. The extinct clade Leptictidae is part of this placental sister clade, indicating that the sister clade survived the KPg event to co-exist in ancient ecosystems during the Paleogene radiation of placentals. Analysing the Cretaceous metatherian Deltatheridium in this character-rich context reveals it is a member of Marsupialia, a finding that extends the minimum age of Marsupialia before the KPg boundary. Numerous shared-derived features from multiple anatomical systems support the assignment of Deltatheridium to Marsupialia. Computed tomography scans of exquisite new specimens better document the marsupial-like dental replacement pattern of Deltatheridium. The new placental sister clade has both Asian and North American species, and is ancestrally characterized by shared derived features such as a hind limb modified for saltatorial locomotion.

The early origin of a birdlike inner ear and the evolution of dinosaurian movement and vocalization.

Reptiles, including birds, exhibit a range of behaviorally relevant adaptations that are reflected in changes to the structure of the inner ear. These adaptations include the capacity for flight and sensitivity to high-frequency sound. We used three-dimensional morphometric analyses of a large sample of extant and extinct reptiles to investigate inner ear correlates of locomotor ability and hearing acuity. Statistical analyses revealed three vestibular morphotypes, best explained by three locomotor categories-quadrupeds, bipeds and simple fliers (including bipedal nonavialan dinosaurs), and high-maneuverability fliers. Troodontids fall with Archaeopteryx among the extant low-maneuverability fliers. Analyses of cochlear shape revealed a single instance of elongation, on the stem of Archosauria. We suggest that this transformation coincided with the origin of both high-pitched juvenile location, alarm, and hatching-synchronization calls and adult responses to them.

A candidate gene analysis and GWAS for genes associated with maternal nondisjunction of chromosome 21.

Human nondisjunction errors in oocytes are the leading cause of pregnancy loss, and for pregnancies that continue to term, the leading cause of intellectual disabilities and birth defects. For the first time, we have conducted a candidate gene and genome-wide association study to identify genes associated with maternal nondisjunction of chromosome 21 as a first step to understand predisposing factors. A total of 2,186 study participants were genotyped on the HumanOmniExpressExome-8v1-2 array. These participants included 749 live birth offspring with standard trisomy 21 and 1,437 parents. Genotypes from the parents and child were then used to identify mothers with nondisjunction errors derived in the oocyte and to establish the type of error (meiosis I or meiosis II). We performed a unique set of subgroup comparisons designed to leverage our previous work suggesting that the etiologies of meiosis I and meiosis II nondisjunction differ for trisomy 21. For the candidate gene analysis, we selected genes associated with chromosome dynamics early in meiosis and genes associated with human global recombination counts. Several candidate genes showed strong associations with maternal nondisjunction of chromosome 21, demonstrating that genetic variants associated with normal variation in meiotic processes can be risk factors for nondisjunction. The genome-wide analysis also suggested several new potentially associated loci, although follow-up studies using independent samples are required.

Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function.

Over the past two centuries, mammalian chewing and related anatomical features have been among the most discussed of all vertebrate evolutionary innovations1-3. Chief among these features are two characters: the dentary-only mandible, and the tribosphenic molar with its triangulated upper cusps and lower talonid basin3-5. The flexible mandibular joint and the unfused symphysis of ancestral mammals-in combination with transformations of the adductor musculature and palate-are thought to have permitted greater mobility of each lower jaw, or hemimandible6,7. Following the appearance of precise dental occlusion near the origin of the mammalian crown8,9, therians evolved a tribosphenic molar with a craggy topography that is presumed to have been used to catch, cut and crush food. Here we describe the ancestral tribosphenic therian chewing stroke, as conserved in the short-tailed opossum Monodelphis domestica: it is a simple symmetrical sequence of lower tooth-row eversion and inversion during jaw opening and closing, respectively, enacted by hemimandibular long-axis rotation. This sequence is coupled with an eversion-inversion rotational grinding stroke. We infer that the ancestral therian chewing stroke relied heavily on long-axis rotation, including symmetrical eversion and inversion (inherited from the first mammaliaforms) as well as a mortar-and-pestle rotational grinding stroke that was inherited from stem therians along with the tribosphenic molar. The yaw-dominated masticatory cycle of primates, ungulates and other bunodont therians is derived; it is necessitated by a secondarily fused jaw symphysis, and permitted by the reduction of high, interlocking cusps10-12. The development of an efficient masticatory system-culminating in the tribosphenic apparatus-allowed early mammals to begin the process of digestion by shearing and crushing food into small boli instead of swallowing larger pieces in the reptilian manner, which necessitates a long, slow and wholly chemical breakdown. The vast diversity of mammalian teeth has emerged from the basic tribosphenic groundplan13.

Jurassic stem-mammal perinates and the origin of mammalian reproduction and growth.

Transformations in morphology, physiology and behaviour along the mammalian stem lineage were accompanied by profound modifications to reproduction and growth, including the emergence of a reproductive strategy characterized by high maternal investment in a small number of offspring1,2 and heterochronic changes in early cranial development associated with the enlargement of the brain3. Because direct fossil evidence of these transitions is lacking, the timing and sequence of these modifications are unknown. Here we present what is, to our knowledge, the first fossil record of pre- or near-hatching young of any non-mammalian synapsid. A large clutch of well-preserved perinates of the tritylodontid Kayentatherium wellesi (Cynodontia, Mammaliamorpha) was found with a presumed maternal skeleton in Early Jurassic sediments of the Kayenta Formation. The single clutch comprises at least 38 individuals, well outside the range of litter sizes documented in extant mammals. This discovery confirms that production of high numbers of offspring represents the ancestral condition for amniotes, and also constrains the timing of a reduction in clutch size along the mammalian stem. Although tiny, the perinates have an overall skull shape that is similar to that of adults, with no allometric lengthening of the face during ontogeny. The only positive allometries are associated with the bones that support the masticatory musculature. Kayentatherium diverged just before a hypothesized pulse of brain expansion that reorganized cranial architecture at the base of Mammaliaformes4-6. The association of a high number of offspring and largely isometric cranial growth in Kayentatherium is consistent with a scenario in which encephalization-and attendant shifts in metabolism and development7,8-drove later changes to mammalian reproduction.

The skull roof tracks the brain during the evolution and development of reptiles including birds.

Major transformations in brain size and proportions, such as the enlargement of the brain during the evolution of birds, are accompanied by profound modifications to the skull roof. However, the hypothesis of concerted evolution of shape between brain and skull roof over major phylogenetic transitions, and in particular of an ontogenetic relationship between specific regions of the brain and the skull roof, has never been formally tested. We performed 3D morphometric analyses to examine the deep history of brain and skull-roof morphology in Reptilia, focusing on changes during the well-documented transition from early reptiles through archosauromorphs, including nonavian dinosaurs, to birds. Non-avialan taxa cluster tightly together in morphospace, whereas Archaeopteryx and crown birds occupy a separate region. There is a one-to-one correspondence between the forebrain and frontal bone and the midbrain and parietal bone. Furthermore, the position of the forebrain-midbrain boundary correlates significantly with the position of the frontoparietal suture across the phylogenetic breadth of Reptilia and during the ontogeny of individual taxa. Conservation of position and identity in the skull roof is apparent, and there is no support for previous hypotheses that the avian parietal is a transformed postparietal. The correlation and apparent developmental link between regions of the brain and bony skull elements are likely to be ancestral to Tetrapoda and may be fundamental to all of Osteichthyes, coeval with the origin of the dermatocranium.

How to Make a Bird Skull: Major Transitions in the Evolution of the Avian Cranium, Paedomorphosis, and the Beak as a Surrogate Hand.

The avian skull is distinctive in its construction and in its function. Much of bird anatomical variety is expressed in the beak; but the beak itself, largely formed of the premaxillary bone, is set upon a shortened face and a bulbous, enlarged braincase. Here, we use original anatomical observations and reconstructions to describe the overall form of the avian skull in a larger context and to provide a general account of the evolutionary transformation from the early dinosaur skull-the skull of an archosaurian macropredator-to that of modern birds. Facial shortening, the enlargement of the braincase around an enlarged brain (with consequential reduction of circumorbital elements and the adductor chamber), and general thinning and looser articulation of bones are trends. Many of these owe to juvenilization or paedomorphosis, something that is abundantly evident from comparison of a juvenile early theropod (Coelophysis) to early avialans like Archaeopteryx Near the avian crown, the premaxilla becomes dramatically enlarged and integrated into the characteristic mobile kinetic system of birds. We posit that this addition of a large element onto the skull may be biomechanically feasible only because of the paedomorphic shortening of the face; and kinesis of the beak only because of the paedomorphic thinning of the bones and loosening of articulations, as played out in reverse during the maturation of Coelophysis Finally, the beak itself becomes elaborated as the hands are integrated into the wing. There are structural, kinematic, and neurological similarities between avian pecking and primate grasping. The ability to precision-select high-quality food against a complex but depauperate background may have permitted crown birds to survive the end-Cretaceous cataclysm by feeding on insects, seeds, and other detritus after the collapse of higher trophic levels in the food web.