Indraloris and Sivaladapis: Miocene adapid primates from the Siwaliks of India and Pakistan

THE primate family Adapidae underwent a major radiation during the Eocene in Europe(1,2) and North America(3,4). Asian and African Eocene mammalian faunas are still poorly known, but there is sufficient evidence to indicate at least a modest radiation of Eocene adapids in Asia(5,6) and probably also in Africa(2). Apart from possible lemuriform and anthropoid primate derivatives, the family Adapidae was thought to have become extinct at the end of the Eocene (middle Tongrian, approximately 37 Myr (refs 2, 7, 8)). We present here new evidence which indicates that at least two genera of adapid primates, Indraloris and Sivaladapis (gen. nov.), survived into the late Miocene of India and Pakistan. These genera are little advanced over Eocene Adapidae in terms of dental adaptations and are apparently south Asian relicts of a much earlier radiation.     

The earliest known fully quadrupedal sirenian.

Modern seacows (manatees and dugongs; Mammalia, Sirenia) are completely aquatic, with flipperlike forelimbs and no hindlimbs. Here I describe Eocene fossils from Jamaica that represent nearly the entire skeleton of a new genus and species of sirenian--the most primitive for which extensive postcranial remains are known. This animal was fully capable of locomotion on land, with four well-developed legs, a multivertebral sacrum, and a strong sacroiliac articulation that could support the weight of the body out of water as in land mammals. Aquatic adaptations show, however, that it probably spent most of its time in the water. Its intermediate form thus illustrates the evolutionary transition between terrestrial and aquatic life. Similar to contemporary primitive cetaceans, it probably swam by spinal extension with simultaneous pelvic paddling, unlike later sirenians and cetaceans, which lost the hindlimbs and enlarged the tail to serve as the main propulsive organ. Together with fossils of later sirenians elsewhere in the world, these new specimens document one of the most marked examples of morphological evolution in the vertebrate fossil record.     

The oldest known anthropoid postcranial fossils and the early evolution of higher primates

The middle Eocene primate family Eosimiidae, which is known from sites in central and eastern China and Myanmar, is central to efforts to reconstruct the origin and early evolution of anthropoid or 'higher' primates (monkeys, apes and humans). Previous knowledge of eosimiid anatomy has been restricted to the dentition and an isolated petrosal bone, and this limited anatomical information has led to conflicting interpretations of early anthropoid phylogeny. Here we describe foot bones of Eosimias from the same middle Eocene sites in China that yield abundant dental remains of this primate. Tarsals of Eosimias show derived anatomical traits that are otherwise restricted to living and fossil anthropoids. These new fossils substantiate the anthropoid status of Eosimias and clarify the phylogenetic position of anthropoids with respect to other major primate clades. Early anthropoids possessed a mosaic of primitive and derived traits in their postcranial skeletons, reflecting their derivation from haplorhine ancestors that retained many prosimian-like features.     

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.     

Interrelationships among primate higher taxa

One of the most controversial issues in primate palaeontology concerns the phylogenetic position of the extinct primate infraorder Adapiformes. During the Eocene, this group of primates of modern aspect possessed a holarctic distribution, and may have been present in the poorly known Palaeogene of Africa. Mainly on the basis of craniodental morphology, at least four hypotheses have been proposed concerning the phylogenetic interrelationships among adapiforms and other primate higher taxa: (1) that adapiforms are ancestral to both lemuriforms (including Lorisoidea) and anthropoids; (2) that adapiforms cannot be shown to possess a special phylogenetic relationship with either lemuriforms or anthropoids; (3) that adapiforms are the sister taxon of lemuriforms; and (4) that Adapiformes is not a natural, monophyletic group, but rather consists of nested clades within the radiation of lemuriforms. Here, we describe features of the ankle and wrist joints of several adapiform taxa that provide an independent test of the preceding hypotheses. These traits suggest that lemuriforms are monophyletic with respect to known adapiforms, but that adapiforms nevertheless are their stem lineage (sensu Ax).     

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.     

Vertebrate faunas and chronology of hominid-bearing sediments east of Lake Rudolf,Kenya

The vertebrate faunas which have been collected from east of Lake Rudolf include hominid remains and the earliest dated stone artefacts known. It is now possible to recognize faunal units and to establish a tentative chronology for observed faunal events. It is suggested here that the faunal sequence at East Rudolf may extend from 4.5 m.y. to about 1.3 m.y. with a significant break between about 4.0 and 2.6 m.y.     

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.     

Eocene global warming events driven by ventilation of oceanic dissolved organic carbon

'Hyperthermals' are intervals of rapid, pronounced global warming known from six episodes within the Palaeocene and Eocene epochs (～65-34 million years (Myr) ago). The most extreme hyperthermal was the ～170 thousand year (kyr) interval of 5-7 °C global warming during the Palaeocene-Eocene Thermal Maximum (PETM, 56?Myr ago). The PETM is widely attributed to massive release of greenhouse gases from buried sedimentary carbon reservoirs, and other, comparatively modest, hyperthermals have also been linked to the release of sedimentary carbon. Here we show, using new 2.4-Myr-long Eocene deep ocean records, that the comparatively modest hyperthermals are much more numerous than previously documented, paced by the eccentricity of Earth's orbit and have shorter durations (～40?kyr) and more rapid recovery phases than the PETM. These findings point to the operation of fundamentally different forcing and feedback mechanisms than for the PETM, involving redistribution of carbon among Earth's readily exchangeable surface reservoirs rather than carbon exhumation from, and subsequent burial back into, the sedimentary reservoir. Specifically, we interpret our records to indicate repeated, large-scale releases of dissolved organic carbon (at least 1,600 gigatonnes) from the ocean by ventilation (strengthened oxidation) of the ocean interior. The rapid recovery of the carbon cycle following each Eocene hyperthermal strongly suggests that carbon was re-sequestered by the ocean, rather than the much slower process of silicate rock weathering proposed for the PETM. Our findings suggest that these pronounced climate warming events were driven not by repeated releases of carbon from buried sedimentary sources, but, rather, by patterns of surficial carbon redistribution familiar from younger intervals of Earth history.     

A novel active pentapeptide from chicken brain identified by antibodies to FMRFamide

The tetrapeptide Phe-Met-Arg-Phe-NH2 (FMRFamide) and peptides structurally related to it, have been isolated from molluscan ganglia. They have widespread actions on both invertebrate and vertebrate tissues and there is increasing evidence that they are an important group of invertebrate peptide neurotransmitters. It is of interest that the primary amino acid sequence of FMRFamide forms the C-terminal tetrapeptide of an enkephalin-like heptapeptide (Met-enkephalin-ArgPhe) isolated from bovine adrenal medulla and striatum. Antisera to FMRFamide have been shown to react in radioimmunoassay and immunohistochemistry with material in the central nervous system of various vertebrate species, but the identity of this material, and in particular its relationship to the opioid heptapeptide, remains uncertain. We have used antibodies specific for the C-terminus of FMRFamide in radioimmunoassays to monitor purification of the material in chicken brain. We describe here the sequence of one of the peptides obtained. It is a biologically active peptide which does not seem to be related to other known vertebrate neuropeptides.     

An arid-adapted middle Pleistocene vertebrate fauna from south-central Australia

How well the ecology, zoogeography and evolution of modern biotas is understood depends substantially on knowledge of the Pleistocene. Australia has one of the most distinctive, but least understood, Pleistocene faunas. Records from the western half of the continent are especially rare. Here we report on a diverse and exceptionally well preserved middle Pleistocene vertebrate assemblage from caves beneath the arid, treeless Nullarbor plain of south-central Australia. Many taxa are represented by whole skeletons, which together serve as a template for identifying fragmentary, hitherto indeterminate, remains collected previously from Pleistocene sites across southern Australia. A remarkable eight of the 23 Nullarbor kangaroos are new, including two tree-kangaroos. The diverse herbivore assemblage implies substantially greater floristic diversity than that of the modern shrub steppe, but all other faunal and stable-isotope data indicate that the climate was very similar to today. Because the 21 Nullarbor species that did not survive the Pleistocene were well adapted to dry conditions, climate change (specifically, increased aridity) is unlikely to have been significant in their extinction.     

The earliest evidence for anatomically modern humans in northwestern Europe

The earliest anatomically modern humans in Europe are thought to have appeared around 43,000-42,000 calendar years before present (43-42 kyr cal BP), by association with Aurignacian sites and lithic assemblages assumed to have been made by modern humans rather than by Neanderthals. However, the actual physical evidence for modern humans is extremely rare, and direct dates reach no farther back than about 41-39 kyr cal BP, leaving a gap. Here we show, using stratigraphic, chronological and archaeological data, that a fragment of human maxilla from the Kent's Cavern site, UK, dates to the earlier period. The maxilla (KC4), which was excavated in 1927, was initially diagnosed as Upper Palaeolithic modern human. In 1989, it was directly radiocarbon dated by accelerator mass spectrometry to 36.4-34.7 kyr cal BP. Using a Bayesian analysis of new ultrafiltered bone collagen dates in an ordered stratigraphic sequence at the site, we show that this date is a considerable underestimate. Instead, KC4 dates to 44.2-41.5 kyr cal BP. This makes it older than any other equivalently dated modern human specimen and directly contemporary with the latest European Neanderthals, thus making its taxonomic attribution crucial. We also show that in 13 dental traits KC4 possesses modern human rather than Neanderthal characteristics; three other traits show Neanderthal affinities and a further seven are ambiguous. KC4 therefore represents the oldest known anatomically modern human fossil in northwestern Europe, fills a key gap between the earliest dated Aurignacian remains and the earliest human skeletal remains, and demonstrates the wide and rapid dispersal of early modern humans across Europe more than 40 kyr ago.     

Head and backbone of the Early Cambrian vertebrate Haikouichthys

Agnathan fish hold a key position in vertebrate evolution, especially regarding the origin of the head and neural-crest-derived tissue. In contrast to amphioxus, lampreys and other vertebrates possess a complex brain and placodes that contribute to well-developed eyes, as well as auditory and olfactory systems. These sensory sytems were arguably a trigger to subsequent vertebrate diversifications. However, although they are known from skeletal impressions in younger Palaeozoic agnathans, information about the earliest records of these systems has been largely wanting. Here we report numerous specimens of the Lower Cambrian vertebrate Haikouichthys ercaicunensis, until now only known from the holotype. Haikouichthys shows significant differences from other fossil agnathans: key features include a small lobate extension to the head, with eyes and possible nasal sacs, as well as what may be otic capsules. A notochord with separate vertebral elements is also identifiable. Phylogenetic analysis indicates that this fish lies within the stem-group craniates. Although Haikouichthys somewhat resembles the ammocoete larva of modern lampreys, this is because of shared general craniate characters; adult lampreys and hagfishes (the cyclostomes if monophyletic) are probably derived in many respects.     

Episodic fresh surface waters in the Eocene Arctic Ocean

It has been suggested, on the basis of modern hydrology and fully coupled palaeoclimate simulations, that the warm greenhouse conditions that characterized the early Palaeogene period (55-45 Myr ago) probably induced an intensified hydrological cycle with precipitation exceeding evaporation at high latitudes. Little field evidence, however, has been available to constrain oceanic conditions in the Arctic during this period. Here we analyse Palaeogene sediments obtained during the Arctic Coring Expedition, showing that large quantities of the free-floating fern Azolla grew and reproduced in the Arctic Ocean by the onset of the middle Eocene epoch (approximately 50 Myr ago). The Azolla and accompanying abundant freshwater organic and siliceous microfossils indicate an episodic freshening of Arctic surface waters during an approximately 800,000-year interval. The abundant remains of Azolla that characterize basal middle Eocene marine deposits of all Nordic seas probably represent transported assemblages resulting from freshwater spills from the Arctic Ocean that reached as far south as the North Sea. The termination of the Azolla phase in the Arctic coincides with a local sea surface temperature rise from approximately 10 degrees C to 13 degrees C, pointing to simultaneous increases in salt and heat supply owing to the influx of waters from adjacent oceans. We suggest that onset and termination of the Azolla phase depended on the degree of oceanic exchange between Arctic Ocean and adjacent seas.     

Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration

The vertebrate visual system can operate over a large range of light intensities. This is possible in part because the sensitivity of photoreceptors decreases approximately in inverse proportion to the background light intensity. This process, called photoreceptor light adaptation, is known to be mediated by a diffusible intracellular messenger, but the identity of the messenger is still unclear. There has been considerable speculation that decreased cytoplasmic Ca2+ concentration (Cai2+) may play a role in light adaptation, and recent experiments in which Ca2+ buffer was incorporated into rod-cells have supported this notion. The extent of the contribution of calcium, however, remains unresolved. We now show that light-dependent changes in sensitivity in amphibian photoreceptors can be abolished by preventing movements of Ca2+ across the outer-segment plasma membrane. These experiments demonstrate that light adaptation in photoreceptors is mediated in cones primarily, and in rods perhaps exclusively, by changes in Cai2+.     

A euprimate skull from the early Eocene of China

The debut of undoubted euprimates (primates of modern aspect) was in the early Eocene, about 55 Myr ago. Since their first appearance, the earliest euprimates can be distinguished as Cantius, Donrussellia and Teilhardina. Nonetheless, the earliest euprimates are primarily known from isolated teeth or fragmentary jaws. Here we describe a partially preserved euprimate skull with nearly complete upper and lower dentition, which represents a new species of Teilhardina and constitutes the first discovery of the genus in Asia. The new species is from the upper section of Lingcha Formation, Hunan Province, China, with an estimated age of 54.97 Myr ago. Morphology and phylogeny analyses reveal that the new species is the most primitive species of Teilhardina, positioned near the root of euprimate radiation. This discovery of the earliest euprimate skull known to date casts new light on the debate concerning the adaptive origin of euprimates, and suggests that the last common ancestor of euprimates was probably a small, diurnal, visually oriented predator.     

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.     

Hagfish embryology with reference to the evolution of the neural crest

Hagfish, which lack both jaws and vertebrae, have long been the subject of intense interest owing to their position at a crucial point in the evolutionary transition to a truly vertebrate body plan. However, unlike the comparatively well characterized vertebrate agnathan lamprey, little is known about hagfish development. The inability to analyse hagfish at early embryonic stages has frustrated attempts to resolve questions with important phylogenetic implications, including fundamental ones relating to the emergence of the neural crest. Here we report the obtainment of multiple pharyngula-stage embryos of the hagfish species Eptatretus burgeri and our preliminary analyses of their early development. We present histological evidence of putative neural crest cells, which appear as delaminated cells that migrate along pathways corresponding to neural crest cells in fish and amphibians. Molecular cloning studies further revealed the expression of several regulatory genes, including cognates of Pax6, Pax3/7, SoxEa and Sox9, suggesting that the hagfish neural crest is specified by molecular mechanisms that are general to vertebrates. We propose that the neural crest emerged as a population of de-epithelialized migratory cells in a common vertebrate ancestor, and suggest that the possibility of classical and molecular embryology in hagfish opens up new approaches to clarifying the evolutionary history of vertebrates.