Using the fossil record to estimate the age of the last common ancestor of extant primates

Divergence times estimated from molecular data often considerably predate the earliest known fossil representatives of the groups studied. For the order Primates, molecular data calibrated with various external fossil dates uniformly suggest a mid-Cretaceous divergence from other placental mammals, some 90 million years (Myr) ago, whereas the oldest known fossil primates are from the basal Eocene epoch (54-55 Myr ago). The common ancestor of primates should be earlier than the oldest known fossils, but adequate quantification is needed to interpret possible discrepancies between molecular and palaeontological estimates. Here we present a new statistical method, based on an estimate of species preservation derived from a model of the diversification pattern, that suggests a Cretaceous last common ancestor of primates, approximately 81.5 Myr ago, close to the initial divergence time inferred from molecular data. It also suggests that no more than 7% of all primate species that have ever existed are known from fossils. The approach unites all the available palaeontological methods of timing evolutionary events: the fossil record, extant species and clade diversification models.     

Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation

Bats (Chiroptera) represent one of the largest and most diverse radiations of mammals, accounting for one-fifth of extant species. Although recent studies unambiguously support bat monophyly and consensus is rapidly emerging about evolutionary relationships among extant lineages, the fossil record of bats extends over 50 million years, and early evolution of the group remains poorly understood. Here we describe a new bat from the Early Eocene Green River Formation of Wyoming, USA, with features that are more primitive than seen in any previously known bat. The evolutionary pathways that led to flapping flight and echolocation in bats have been in dispute, and until now fossils have been of limited use in documenting transitions involved in this marked change in lifestyle. Phylogenetically informed comparisons of the new taxon with other bats and non-flying mammals reveal that critical morphological and functional changes evolved incrementally. Forelimb anatomy indicates that the new bat was capable of powered flight like other Eocene bats, but ear morphology suggests that it lacked their echolocation abilities, supporting a 'flight first' hypothesis for chiropteran evolution. The shape of the wings suggests that an undulating gliding-fluttering flight style may be primitive for bats, and the presence of a long calcar indicates that a broad tail membrane evolved early in Chiroptera, probably functioning as an additional airfoil rather than as a prey-capture device. Limb proportions and retention of claws on all digits indicate that the new bat may have been an agile climber that employed quadrupedal locomotion and under-branch hanging behaviour.     

Tunicates and not cephalochordates are the closest living relatives of vertebrates

Tunicates or urochordates (appendicularians, salps and sea squirts), cephalochordates (lancelets) and vertebrates (including lamprey and hagfish) constitute the three extant groups of chordate animals. Traditionally, cephalochordates are considered as the closest living relatives of vertebrates, with tunicates representing the earliest chordate lineage. This view is mainly justified by overall morphological similarities and an apparently increased complexity in cephalochordates and vertebrates relative to tunicates. Despite their critical importance for understanding the origins of vertebrates, phylogenetic studies of chordate relationships have provided equivocal results. Taking advantage of the genome sequencing of the appendicularian Oikopleura dioica, we assembled a phylogenomic data set of 146 nuclear genes (33,800 unambiguously aligned amino acids) from 14 deuterostomes and 24 other slowly evolving species as an outgroup. Here we show that phylogenetic analyses of this data set provide compelling evidence that tunicates, and not cephalochordates, represent the closest living relatives of vertebrates. Chordate monophyly remains uncertain because cephalochordates, albeit with a non-significant statistical support, surprisingly grouped with echinoderms, a hypothesis that needs to be tested with additional data. This new phylogenetic scheme prompts a reappraisal of both morphological and palaeontological data and has important implications for the interpretation of developmental and genomic studies in which tunicates and cephalochordates are used as model animals.     

Skull of the large non-macrostomatan snake Yurlunggur from the Australian Oligo-Miocene

Understanding the origin and early evolution of snakes from lizards depends on accurate morphological knowledge of the skull in basal lineages, but fossil specimens of archaic snakes have been rare, and either fragmentary or difficult to study as a result of compression by enclosing sediments. A number of Cenozoic fossil snakes from Australia have vertebral morphology diagnostic of an extinct group, Madtsoiidae, that was widespread in Gondwana from mid-Cretaceous (Cenomanian) to Eocene times, and also reached Europe in the late Cretaceous period. Despite this long history, only about half the skull is known from the best-known species Wonambi naracoortensis, and the few known cranial elements of other species have added little further evidence for phylogenetic relationships. Conflicting hypotheses have been proposed for their relationships and evolutionary significance, either as basal ophidians with many ancestral (varanoid- or mosasaur-like) features, or advanced (macrostomatan) alethinophidians of little relevance to snake origins. Here I report two partial skeletons referred to Yurlunggur, from the late Oligocene and early Miocene of northern Australia, which together represent almost the complete skull and mandible. The exceptionally preserved skulls provide new evidence linking Yurlunggur with Wonambi and other madtsoiids, falsifying predictions of the macrostomatan hypothesis, and supporting the exclusion of Madtsoiidae from the clade including all extant snakes.     

First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy

The phylogenetic relationships of living tarsiers and extinct omomyid primates are critical for deciphering the origin and relationships of primate higher taxa, particularly anthropoids. Three competing phylogenetic hypotheses are: (1) tarsiers are most closely related to early Cenozoic Omomyidae, particularly genera such as Necrolemur from the late Eocene of Europe; (2) tarsiers share a more recent common ancestry with anthropoids than they do with any known omomyid; (3) tarsiers and/or omomyids are most closely related to strepsirhines. The anatomy of four skulls of the early Eocene omomyid Shoshonius cooperi--the first cranial material recovered for this genus--strongly suggests that Shoshonius shares a more recent common ancestry with Tarsius than do either anthropoids or other Eocene omomyids for which cranial anatomy is known. If the primate suborder Haplorhini (anthropoids, omomyids, tarsiids) is monophyletic, the phylogenetic position of Shoshonius requires that anthropoids and Tarsius diverged by at least the early Eocene, some 15 million years before the first appearance of anthropoids in the fossil record.     

The delayed rise of present-day mammals

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.     

A Cretaceous terrestrial snake with robust hindlimbs and a sacrum

It has commonly been thought that snakes underwent progressive loss of their limbs by gradual diminution of their use. However, recent developmental and palaeontological discoveries suggest a more complex scenario of limb reduction, still poorly documented in the fossil record. Here we report a fossil snake with a sacrum supporting a pelvic girdle and robust, functional legs outside the ribcage. The new fossil, from the Upper Cretaceous period of Patagonia, fills an important gap in the evolutionary progression towards limblessness because other known fossil snakes with developed hindlimbs, the marine Haasiophis, Pachyrhachis and Eupodophis, lack a sacral region. Phylogenetic analysis shows that the new fossil is the most primitive (basal) snake known and that all other limbed fossil snakes are closer to the more advanced macrostomatan snakes, a group including boas, pythons and colubroids. The new fossil retains several features associated with a subterranean or surface dwelling life that are also present in primitive extant snake lineages, supporting the hypothesis of a terrestrial rather than marine origin of snakes.     

Early human occupation of the Red Sea coast of Eritrea during the last interglacial

The geographical origin of modern humans is the subject of ongoing scientific debate. The 'multiregional evolution' hypothesis argues that modern humans evolved semi-independently in Europe, Asia and Africa between 100,000 and 40,000 years ago, whereas the 'out of Africa' hypothesis contends that modern humans evolved in Africa between 200 and 100 kyr ago, migrating to Eurasia at some later time. Direct palaeontological, archaeological and biological evidence is necessary to resolve this debate. Here we report the discovery of early Middle Stone Age artefacts in an emerged reef terrace on the Red Sea coast of Eritrea, which we date to the last interglacial (about 125 kyr ago) using U-Th mass spectrometry techniques on fossil corals. The geological setting of these artefacts shows that early humans occupied coastal areas and exploited near-shore marine food resources in East Africa by this time. Together with similar, tentatively dated discoveries from South Africa this is the earliest well-dated evidence for human adaptation to a coastal marine environment, heralding an expansion in the range and complexity of human behaviour from one end of Africa to the other. This new, wide-spread adaptive strategy may, in part, signal the onset of modern human behaviour, which supports an African origin for modern humans by 125 kyr ago.     

An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish

Comparative analyses of Hox gene expression and regulation in teleost fish and tetrapods support the long-entrenched notion that the distal region of tetrapod limbs, containing the wrist, ankle and digits, is an evolutionary novelty. Data from fossils support the notion that the unique features of tetrapod limbs were assembled over evolutionary time in the paired fins of fish. The challenge in linking developmental and palaeontological approaches has been that developmental data for fins and limbs compare only highly derived teleosts and tetrapods; what is lacking are data from extant taxa that retain greater portions of the fin skeletal morphology considered primitive to all bony fish. Here, we report on the expression and function of genes implicated in the origin of the autopod in a basal actinopterygian, Polyodon spathula. Polyodon exhibits a late-phase, inverted collinear expression of 5' HoxD genes, a pattern of expression long considered a developmental hallmark of the autopod and shown in tetrapods to be controlled by a 'digit enhancer' region. These data show that aspects of the development of the autopod are primitive to tetrapods and that the origin of digits entailed the redeployment of ancient patterns of gene activity.     

Persistent near-tropical warmth on the Antarctic continent during the early Eocene epoch

The warmest global climates of the past 65 million years occurred during the early Eocene epoch (about 55 to 48 million years ago), when the Equator-to-pole temperature gradients were much smaller than today and atmospheric carbon dioxide levels were in excess of one thousand parts per million by volume. Recently the early Eocene has received considerable interest because it may provide insight into the response of Earth's climate and biosphere to the high atmospheric carbon dioxide levels that are expected in the near future as a consequence of unabated anthropogenic carbon emissions. Climatic conditions of the early Eocene 'greenhouse world', however, are poorly constrained in critical regions, particularly Antarctica. Here we present a well-dated record of early Eocene climate on Antarctica from an ocean sediment core recovered off the Wilkes Land coast of East Antarctica. The information from biotic climate proxies (pollen and spores) and independent organic geochemical climate proxies (indices based on branched tetraether lipids) yields quantitative, seasonal temperature reconstructions for the early Eocene greenhouse world on Antarctica. We show that the climate in lowland settings along the Wilkes Land coast (at a palaeolatitude of about 70° south) supported the growth of highly diverse, near-tropical forests characterized by mesothermal to megathermal floral elements including palms and Bombacoideae. Notably, winters were extremely mild (warmer than 10?°C) and essentially frost-free despite polar darkness, which provides a critical new constraint for the validation of climate models and for understanding the response of high-latitude terrestrial ecosystems to increased carbon dioxide forcing.     

Late Cretaceous relatives of rabbits, rodents, and other extant eutherian mammals.

Extant eutherian mammals and their most recent common ancestor constitute the crown group Placentalia. This taxon, plus all extinct taxa that share a more recent common ancestor with placentals than they do with Metatheria (including marsupials), constitute Eutheria. The oldest well documented eutherian-dominated fauna in the world is Dzharakuduk, Uzbekistan. Among eutherians that it yields is Kulbeckia, an 85-90-Myr-old member of Zalambdalestidae (a family of Late Cretaceous Asian eutherians). This extends Zalambdalestidae back by some 10 million years from sites in the Gobi Desert, Mongolia. A phylogenetic analysis of well described Late Cretaceous eutherians strongly supports Zalambdalestidae, less strongly supports 'Zhelestidae' (a Late Cretaceous clade related to Tertiary ungulates), but does not support Asioryctitheria (a group of Late Cretaceous Asian eutherians). A second analysis incorporating placentals from clades that include rodents (Tribosphenomys), lagomorphs (Mimotona) and archaic ungulates (Protungulatum and Oxyprimus) strongly supports Zalambdalestidae in a clade with Glires (rabbits, rodents and extinct relatives) and less strongly 'Zhelestidae' within a clade that includes archaic ungulates ('condylarths'). This argues that some Late Cretaceous eutherians belong within the crown group Placentalia. The ages of these taxa are in line with molecularly based estimates of 64-104 Myr ago (median 84 Myr ago) for the superordinal diversification of some placentals, but provide no support for a Late Cretaceous diversification of extant placental orders.     

A new troodontid dinosaur from China with avian-like sleeping posture

Discovering evidence of behaviour in fossilized vertebrates is rare. Even rarer is evidence of behaviour in non-avialan dinosaurs that directly relates to stereotypical behaviour seen in extant birds (avians) and not previously predicted in non-avialan dinosaurs. Here we report the discovery of a new troodontid taxon from the Early Cretaceous Yixian Formation of western Liaoning, China. Numerous other three-dimensionally preserved vertebrate fossils have been recovered recently at this locality, including some specimens preserving behavioural information. The new troodontid preserves several features that have been implicated in avialan origins. Notably, the specimen is preserved in the stereotypical sleeping or resting posture found in extant Aves. Evidence of this behaviour outside of the crown group Aves further demonstrates that many bird features occurred early in dinosaurian evolution.     

Post-Jurassic mammal-like reptile from the Palaeocene.

Mammal-like reptiles of the order Therapsida document the emergence of mammals from more primitive synapsids and are of unique zoological and palaeontological interest on that account. Therapsids, first appearing in the Early Permian, were thought to become extinct in the Middle Jurassic, soon after the Late Triassic origin of mammals. Here, however, we report the discovery of a therapsid from the late Palaeocene, 100 million years younger than the youngest previous occurrence of the order. This discovery nearly doubles the stratigraphic range of therapsids and furnishes their first record from the Cenozoic. The documenting fossils, an incomplete dentary containing three teeth, and four isolated teeth from other, conspecific individuals (Fig. 1), are from the Paskapoo Formation, at Cochrane, Alberta, Canada, from beds yielding a diverse mammalian fauna of early Tiffanian age. These specimens are catalogued in the collections of the University of Alberta Laboratory for Vertebrate Paleontology (UALVP) and provide the basis for a new taxon, as named and described below: (see text)     

Dating the origin of the Orchidaceae from a fossil orchid with its pollinator

Since the time of Darwin, evolutionary biologists have been fascinated by the spectacular adaptations to insect pollination exhibited by orchids. However, despite being the most diverse plant family on Earth, the Orchidaceae lack a definitive fossil record and thus many aspects of their evolutionary history remain obscure. Here we report an exquisitely preserved orchid pollinarium (of Meliorchis caribea gen. et sp. nov.) attached to the mesoscutellum of an extinct stingless bee, Proplebeia dominicana, recovered from Miocene amber in the Dominican Republic, that is 15-20 million years (Myr) old. This discovery constitutes both the first unambiguous fossil of Orchidaceae and an unprecedented direct fossil observation of a plant-pollinator interaction. By applying cladistic methods to a morphological character matrix, we resolve the phylogenetic position of M. caribea within the extant subtribe Goodyerinae (subfamily Orchidoideae). We use the ages of other fossil monocots and M. caribea to calibrate a molecular phylogenetic tree of the Orchidaceae. Our results indicate that the most recent common ancestor of extant orchids lived in the Late Cretaceous (76-84 Myr ago), and also suggest that the dramatic radiation of orchids began shortly after the mass extinctions at the K/T boundary. These results further support the hypothesis of an ancient origin for Orchidaceae.     

Evidence for echolocation in the oldest known bats

The earliest-known bats are represented by excellent fossil material, including virtually complete skeletons of Icaronycteris index from the early Eocene (50 Myr BP) of western Wyoming and Palaeochiropteryx tupaiodon from the middle Eocene (45 Myr BP) 'Grube Messel' of western Germany. These taxa have been closely allied with Recent Microchiroptera, a suborder of diverse bats noted for their powers of ultrasonic echolocation. A problem with this relationship is the alleged absence in the Eocene forms of specializations in the auditory region and other aspects of the skeletal system. It has been proposed, therefore, that the oldest bats are members of a group more primitive and possibly ancestral to the Microchiroptera and the visually oriented Megachiroptera. Previously undescribed specimens now show, however, that Icaronycteris and Palaeochiropteryx share special basicranial features with microchiropterans which suggest comparable refinement of ultrasonic echolocation. These results support the theory that a sophisticated sonar system was present in the earliest records of microchiropteran history.     

Late middle Eocene epoch of Libya yields earliest known radiation of African anthropoids

Reconstructing the early evolutionary history of anthropoid primates is hindered by a lack of consensus on both the timing and biogeography of anthropoid origins. Some prefer an ancient (Cretaceous) origin for anthropoids in Africa or some other Gondwanan landmass, whereas others advocate a more recent (early Cenozoic) origin for anthropoids in Asia, with subsequent dispersal of one or more early anthropoid taxa to Africa. The oldest undoubted African anthropoid primates described so far are three species of the parapithecid Biretia from the late middle Eocene Bir El Ater locality of Algeria and the late Eocene BQ-2 site in the Fayum region of northern Egypt. Here we report the discovery of the oldest known diverse assemblage of African anthropoids from the late middle Eocene Dur At-Talah escarpment in central Libya. The primate assemblage from Dur At-Talah includes diminutive species pertaining to three higher-level anthropoid clades (Afrotarsiidae, Parapithecidae and Oligopithecidae) as well as a small species of the early strepsirhine primate Karanisia. The high taxonomic diversity of anthropoids at Dur At-Talah indicates either a much longer interval of anthropoid evolution in Africa than is currently documented in the fossil record or the nearly synchronous colonization of Africa by multiple anthropoid clades at some time during the middle Eocene epoch.     

Possible methane-induced polar warming in the early Eocene

Reconstructions of early Eocene climate depict a world in which the polar environments support mammals and reptiles, deciduous forests, warm oceans and rare frost conditions. At the same time, tropical sea surface temperatures are interpreted to have been the same as or slightly cooler than present values. The question of how to warm polar regions of Earth without noticeably warming the tropics remains unresolved; increased amounts of greenhouse gases would be expected to warm all latitudes equally. Oceanic heat transport has been postulated as a mechanism for heating high latitudes, but it is difficult to explain the dynamics that would achieve this. Here we consider estimates of Eocene wetland areas and suggest that the flux of methane, an important greenhouse gas, may have been substantially greater during the Eocene than at present. Elevated methane concentrations would have enhanced early Eocene global warming, and also might specifically have prevented severe winter cooling of polar regions because of the potential of atmospheric methane to promote the formation of optically thick, polar stratospheric ice clouds.     

Earliest known simian primate found in Algeria.

The record of early fossil Simiiformes (Anthropoidea) from the Late Eocene and Early Oligocene of Africa and the Arabian Peninsula has increased dramatically in recent years. We report here the discovery of a new, diminutive and much older (Early or Middle Eocene) simian from an Algerian locality, Glib Zegdou. This species is smaller than any other living or fossil African simiiform. Derived similarities shared with Aegyptopithecus suggest that the new genus is more closely related to propliopithecines than to oligopithecines, implying that these two subfamilies differentiated during the Early Eocene. The new discovery confirms predictions about the great antiquity of Simiiformes and emphasizes a long and endemic African history for higher primates.     

A stem batrachian from the Early Permian of Texas and the origin of frogs and salamanders

The origin of extant amphibians (Lissamphibia: frogs, salamanders and caecilians) is one of the most controversial questions in vertebrate evolution, owing to large morphological and temporal gaps in the fossil record. Current discussions focus on three competing hypotheses: a monophyletic origin within either Temnospondyli or Lepospondyli, or a polyphyletic origin with frogs and salamanders arising among temnospondyls and caecilians among the lepospondyls. Recent molecular analyses are also controversial, with estimations for the batrachian (frog-salamander) divergence significantly older than the palaeontological evidence supports. Here we report the discovery of an amphibamid temnospondyl from the Early Permian of Texas that bridges the gap between other Palaeozoic amphibians and the earliest known salientians and caudatans from the Mesozoic. The presence of a mosaic of salientian and caudatan characters in this small fossil makes it a key taxon close to the batrachian (frog and salamander) divergence. Phylogenetic analysis suggests that the batrachian divergence occurred in the Middle Permian, rather than the late Carboniferous as recently estimated using molecular clocks, but the divergence with caecilians corresponds to the deep split between temnospondyls and lepospondyls, which is congruent with the molecular estimates.     

Cooler winters as a possible cause of mass extinctions at the Eocene/Oligocene boundary

The Eocene/Oligocene boundary, at about 33.7 Myr ago, marks one of the largest extinctions of marine invertebrates in the Cenozoic period. For example, turnover of mollusc species in the US Gulf coastal plain was over 90% at this time. A temperature change across this boundary--from warm Eocene climates to cooler conditions in the Oligocene--has been suggested as a cause of this extinction event, but climate reconstructions have not provided support for this hypothesis. Here we report stable oxygen isotope measurements of aragonite in fish otoliths--ear stones--collected across the Eocene/Oligocene boundary. Palaeo-temperatures reconstructed from mean otolith oxygen isotope values show little change through this interval, in agreement with previous studies. From incremental microsampling of otoliths, however, we can resolve the seasonal variation in temperature, recorded as the otoliths continue to accrete new material over the life of the fish. These seasonal data suggest that winters became about 4 degrees C colder across the Eocene/Oligocene boundary. We suggest that temperature variability, rather than change in mean annual temperature, helped to cause faunal turnover during this transition.