Robert J. Asher

Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny

The fossil record suggests a rapid radiation of placental mammals following the Cretaceous–Paleogene (K–Pg) mass extinction 65 million years ago (Ma); nevertheless, molecular time estimates, while highly variable, are generally much older. Early molecular studies suffer from inadequate dating methods, reliance on the molecular clock, and simplistic and over-confident interpretations of the fossil record. More recent studies have used Bayesian dating methods that circumvent those issues, but the use of limited data has led to large estimation uncertainties, precluding a decisive conclusion on the timing of mammalian diversifications. Here we use a powerful Bayesian method to analyse 36 nuclear genomes and 274 mitochondrial genomes (20.6 million base pairs), combined with robust but flexible fossil calibrations. Our posterior time estimates suggest that marsupials diverged from eutherians 168–178 Ma, and crown Marsupialia diverged 64–84 Ma. Placentalia diverged 88–90 Ma, and present-day placental orders (except Primates and Xenarthra) originated in a ∼20 Myr window (45–65 Ma) after the K–Pg extinction. Therefore we reject a pre K–Pg model of placental ordinal diversification. We suggest other infamous instances of mismatch between molecular and palaeontological divergence time estimates will be resolved with this same approach.

Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary.

Estimates of the time of origin for placental mammals from DNA studies span nearly the duration of the Cretaceous period (145 to 65 million years ago), with a maximum of 129 million years ago and a minimum of 78 million years ago. Palaeontologists too are divided on the timing. Some support a deep Cretaceous origin by allying certain middle Cretaceous fossils (97–90 million years old) from Uzbekistan with modern placental lineages, whereas others support the origin of crown group Placentalia near the close of the Cretaceous. This controversy has yet to be addressed by a comprehensive phylogenetic analysis that includes all well-known Cretaceous fossils and a wide sample of morphology among Tertiary and recent placentals. Here we report the discovery of a new well-preserved mammal from the Late Cretaceous of Mongolia and a broad-scale phylogenetic analysis. Our results exclude Cretaceous fossils from Placentalia, place the origin of Placentalia near the Cretaceous/Tertiary (K/T) boundary in Laurasia rather than much earlier within the Cretaceous in the Southern Hemisphere, and place afrotherians and xenarthrans in a nested rather than a basal position within Placentalia.

Relationships of Endemic African Mammals and Their Fossil Relatives Based on Morphological and Molecular Evidence

Analyses of anatomical and DNA sequence data run on a parallel supercomputer that include fossil taxa support the inclusion of tenrecs and golden moles in the Afrotheria, an endemic African clade of placental mammals. According to weighting schemes of morphological and molecular data that maximize congruence, extinct members of the afrotherian crown group include embrithopods, Plesiorycteropus, desmostylians, and the “condylarths” Hyopsodus, Meniscotherium, and possibly Phenacodus. By influencing the optimization of anatomical characters, molecular data have a large influence on the relationships of several extinct taxa. The inclusion of fossils and morphological data increases support for an elephant-sea cow clade within Paenungulata and identifies ancient, northern elements of a clade whose living members in contrast suggest an historically Gondwanan distribution. In addition, maximally congruent topologies support the position of Afrotheria as well-nested, not basal, within Placentalia. This pattern does not accord with the recent hypothesis that the divergence of placental mammals co-occurred with the tectonic separation of Africa and South America.

The Eutherian Mammal Maelestes gobiensis from the Late Cretaceous of Mongolia and the phylogeny of cretaceous eutheria

Abstract Maelestes gobiensis Wible et al., 2007, is the second new eutherian mammal to be named from the rich Mongolian Late Cretaceous locality of Ukhaa Tolgod, Ukhaatherium nessovi Novacek et al., 1997, being the first. Maelestes is only the seventh Late Cretaceous eutherian known from the skull and the upper and lower dentitions, and the fifth known from some postcranial elements. The type and only known specimen, PSS-MAE 607, is described and illustrated in detail. The type is amended to include: an incomplete skull, left dentary, atlas, axis, last cervical and first 11 thoracic vertebrae, 11 partial ribs, incomplete scapula, clavicle, humerus, and proximal radius and ulna. An astragalus on a separate block was referred to Maelestes by Wible et al. (2007), but it is too large to belong to this taxon and is removed from the isotype. Several corrections and updates are made to the phylogenetic analysis of Wible et al. (2007). The original analysis and the one in this report include 408 morphological characters (127 dental, 212 cranial, and 69 postcranial) in Maelestes along with 68 other taxa (four stem therians, three metatherians, 31 Cretaceous eutherians, 20 extinct Tertiary placentals, and 11 extant placentals). Maelestes is identified as a member of Cimolestidae sensu Kielan-Jaworowska et al. (2004) along with the slightly younger and poorer known North American taxa Batodon Marsh, 1892, and Cimolestes Marsh, 1889. Cimolestidae, in turn, is grouped with Asioryctitheria sensu Archibald and Averianov (2006), which includes monophyletic Mongolian and Uzbekistani clades. The other principal Late Cretaceous clades are: a Laurasian Zhelestidae; Paranyctoides Fox, 1979 (North American and Uzbekistan) + Eozhelestes Nessov, 1997 (Uzbekistan); and an Asian Zalambdalestidae. In contrast to some previous analyses, but in common with Wible et al. (2007), no Cretaceous eutherians are identified as members of any placental group.

The new framework for understanding placental mammal evolution.

An unprecedented level of confidence has recently crystallized around a new hypothesis of how living placental mammals share a pattern of common descent. The major groups are afrotheres (e.g., aardvarks, elephants), xenarthrans (e.g., anteaters, sloths), laurasiatheres (e.g., horses, shrews), and euarchontoglires (e.g., humans, rodents). Compared with previous hypotheses this tree is remarkably stable; however, some uncertainty persists about the location of the placental root, and (for example) the position of bats within laurasiatheres, of sea cows and aardvarks within afrotheres, and of dermopterans within euarchontoglires. A variety of names for sub‐clades within the new placental mammal tree have been proposed, not all of which follow conventions regarding priority and stability. More importantly, the new phylogenetic framework enables the formulation of new hypotheses and testing thereof, for example regarding the possible developmental dichotomy that seems to distinguish members of the newly identified southern and northern radiations of living placental mammals.

Constraints on the timescale of animal evolutionary history

Dating the tree of life is a core endeavor in evolutionary biology. Rates of evolution are fundamental to nearly every evolutionary model and process. Rates need dates. There is much debate on the most appropriate and reasonable ways in which to date the tree of life, and recent work has highlighted some confusions and complexities that can be avoided. Whether phylogenetic trees are dated after they have been established, or as part of the process of tree finding, practitioners need to know which calibrations to use. We emphasize the importance of identifying crown (not stem) fossils, levels of confidence in their attribution to the crown, current chronostratigraphic precision, the primacy of the host geological formation and asymmetric confidence intervals. Here we present calibrations for 88 key nodes across the phylogeny of animals, ranging from the root of Metazoa to the last common ancestor of Homo sapiens. Close attention to detail is constantly required: for example, the classic bird-mammal date (base of crown Amniota) has often been given as 310-315 Ma; the 2014 international time scale indicates a minimum age of 318 Ma. Michael J. Benton. School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, U.K. mike.benton@bristol.ac.uk Philip C.J. Donoghue. School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, U.K. phil.donoghue@bristol.ac.uk Robert J. Asher, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, U.K. r.asher@zoo.cam.ac.uk Matt Friedman, Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, OX1 3AN, U.K. mattf@earth.ox.ac.uk Thomas J. Near, Department of Ecology and Evolutionary Biology, Yale University, P. O. Box 208106, 165 Prospect Street, New Haven, CT 06520-8106, U.S.A. thomas.near@yale.edu Jakob Vinther. School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, U.K. jakob.vinther@bristol.ac.uk PE Article Number: 18.1.1FC Copyright: Society for Vertebrate Paleontology February 2015 Submission: 1 August 2013. Acceptance: 7 December 2014 Benton, Michael J., Donoghue, Philip C.J., Asher, Robert J., Friedman, Matt, Near, Thomas J., and Vinther, Jakob. 2015. Constraints on the timescale of animal evolutionary history. Palaeontologia Electronica 18.1.1FC; 1-106; palaeo-electronica.org/content/fc-1 Calibrations published in the Fossil Calibration Series are accessioned into the Fossil Calibration Database (www.fossilcalibrations.org). The Database is a dynamic tool for finding up-to-date calibrations, and calibration data will be updated and annotated as interpretations change. In contrast, the Fossil Calibration papers are a permanent published record of the information on which the calibrations were originally based. Please refer to the Database for the latest data. BENTON ET AL.: ANIMAL HISTORY TIMESCALE

Dental eruption in afrotherian mammals

BackgroundAfrotheria comprises a newly recognized clade of mammals with strong molecular evidence for its monophyly. In contrast, morphological data uniting its diverse constituents, including elephants, sea cows, hyraxes, aardvarks, sengis, tenrecs and golden moles, have been difficult to identify. Here, we suggest relatively late eruption of the permanent dentition as a shared characteristic of afrotherian mammals. This characteristic and other features (such as vertebral anomalies and testicondy) recall the phenotype of a human genetic pathology (cleidocranial dysplasia), correlations with which have not been explored previously in the context of character evolution within the recently established phylogeny of living mammalian clades.ResultsAlthough data on the absolute timing of eruption in sengis, golden moles and tenrecs are still unknown, craniometric comparisons for ontogenetic series of these taxa show that considerable skull growth takes place prior to the complete eruption of the permanent cheek teeth. Specimens showing less than half (sengis, golden moles) or two-thirds (tenrecs, hyraxes) of their permanent cheek teeth reach or exceed the median jaw length of conspecifics with a complete dentition. With few exceptions, afrotherians are closer to median adult jaw length with fewer erupted, permanent cheek teeth than comparable stages of non-afrotherians. Manatees (but not dugongs), elephants and hyraxes with known age data show eruption of permanent teeth late in ontogeny relative to other mammals. While the occurrence of delayed eruption, vertebral anomalies and other potential afrotherian synapomorphies resemble some symptoms of a human genetic pathology, these characteristics do not appear to covary significantly among mammalian clades.ConclusionMorphological characteristics shared by such physically disparate animals such as elephants and golden moles are not easy to recognize, but are now known to include late eruption of permanent teeth, in addition to vertebral anomalies, testicondy and other features. Awareness of their possible genetic correlates promises insight into the developmental basis of shared morphological features of afrotherians and other vertebrates.

Nomenclature and placental mammal phylogeny

An issue arising from recent progress in establishing the placental mammal Tree of Life concerns the nomenclature of high-level clades. Fortunately, there are now several well-supported clades among extant mammals that require unambiguous, stable names. Although the International Code of Zoological Nomenclature does not apply above the Linnean rank of family, and while consensus on the adoption of competing systems of nomenclature does not yet exist, there is a clear, historical basis upon which to arbitrate among competing names for high-level mammalian clades. Here, we recommend application of the principles of priority and stability, as laid down by G.G. Simpson in 1945, to discriminate among proposed names for high-level taxa. We apply these principles to specific cases among placental mammals with broad relevance for taxonomy, and close with particular emphasis on the Afrotherian family Tenrecidae. We conclude that no matter how reconstructions of the Tree of Life change in years to come, systematists should apply new names reluctantly, deferring to those already published and maximizing consistency with existing nomenclature.

Skeletal development in sloths and the evolution of mammalian vertebral patterning

Mammals show a very low level of variation in vertebral count, particularly in the neck. Phenotypes exhibited at various stages during the development of the axial skeleton may play a key role in testing mechanisms recently proposed to explain this conservatism. Here, we provide osteogenetic data that identify developmental criteria with which to recognize cervical vs. noncervical vertebrae in mammals. Except for sloths, all mammals show the late ossification of the caudal-most centra in the neck after other centra and neural arches. In sloths with 8–10 ribless neck vertebrae, the caudal-most neck centra ossify early, matching the pattern observed in cranial thoracic vertebrae of other mammals. Accordingly, we interpret the ribless neck vertebrae of three-toed sloths caudal to V7 as thoracic based on our developmental criterion. Applied to the unusual vertebral phenotype of long-necked sloths, these data support the interpretation that elements of the axial skeleton with origins from distinct mesodermal tissues have repatterned over the course of evolution.

Exceptionally preserved North American Paleogene metatherians: adaptations and discovery of a major gap in the opossum fossil record

A major gap in our knowledge of the evolution of marsupial mammals concerns the Paleogene of the northern continents, a critical time and place to link the early history of metatherians in Asia and North America with the more recent diversification in South America and Australia. We studied new exceptionally well-preserved partial skeletons of the Early Oligocene fossil Herpetotherium from the White River Formation in Wyoming, which allowed us to test the relationships of this taxon and examine its adaptations. Herpetotheriidae, with a fossil record extending from the Cretaceous to the Miocene, has traditionally been allied with opossums (Didelphidae) based on fragmentary material, mainly dentitions. Analysis of the new material reveals that several aspects of the cranial and postcranial anatomy, some of which suggests a terrestrial lifestyle, distinguish Herpetotherium from opossums. We found that Herpetotherium is the sister group to the crown group Marsupialia and is not a stem didelphid. Combination of the new palaeontological data with molecular divergence estimates, suggests the presence of a long undocumented gap in the fossil record of opossums extending some 45 Myr from the Early Miocene to the Cretaceous.