Ancient Mitogenomes Reveal the Maternal Genetic History of East Asian Dogs.

Recent studies have suggested that dogs were domesticated during the Last Glacial Maximum (LGM) in Siberia, which contrasts with previous proposed domestication centers (e.g. Europe, the Middle East, and East Asia). Ancient DNA provides a powerful resource for the study of mammalian evolution and has been widely used to understand the genetic history of domestic animals. To understand the maternal genetic history of East Asian dogs, we have made a complete mitogenome dataset of 120 East Asian canids from 38 archaeological sites, including 102 newly sequenced from 12.9 to 1 ka BP (1,000 years before present). The majority (112/119, 94.12%) belonged to haplogroup A, and half of these (55/112, 49.11%) belonged to sub-haplogroup A1b. Most existing mitochondrial haplogroups were present in ancient East Asian dogs. However, mitochondrial lineages in ancient northern dogs (northeastern Eurasia and northern East Asia) were deeper and older than those in southern East Asian dogs. Results suggests that East Asian dogs originated from northeastern Eurasian populations after the LGM, dispersing in two possible directions after domestication. Western Eurasian (Europe and the Middle East) dog maternal ancestries genetically influenced East Asian dogs from approximately 4 ka BP, dramatically increasing after 3 ka BP, and afterwards largely replaced most primary maternal lineages in northern East Asia. Additionally, at least three major mitogenome sub-haplogroups of haplogroup A (A1a, A1b, and A3) reveal at least two major dispersal waves onto the Qinghai-Tibet Plateau in ancient times, indicating eastern (A1b and A3) and western (A1a) Eurasian origins.

Uncovering widespread Anthropocene dietary shifts in Chinese large mammalian herbivores.

The Anthropocene's human-dominated habitat expansion endangers global biodiversity. However, large mammalian herbivores experienced few extinctions during the 20th century, hinting at potentially overlooked ecological responses of a group sensitive to global change. Using dental microwear as a proxy, we studied large herbivore dietary niches over a century across mainland China before (1880s-1910s) and after (1970s-1990s) the human population explosion. We uncovered widespread and significant shifts (interspecific microwear differences increased and intraspecific microwear dispersion expanded) within dietary niches linked to geographical areas with rapid industrialization and population growth in eastern China. By contrast, in western China, where human population growth was slower, we found no indications of shifts in herbivore dietary niches. Further regression analysis links the intensity of microwear changes to human land-use expansion. These analyses highlight dietary adjustments of large herbivores as a likely key factor in their adaptation across a century of large-scale human-driven changes.

Phylogeny and paleobiogeography of the enigmatic North American primate Ekgmowechashala illuminated by new fossils from Nebraska (USA) and Guangxi Zhuang Autonomous Region (China).

Ekgmowechashala is a poorly documented but very distinctive primate known only from the late early Oligocene (early Arikareean) of western North America. Because of its highly autapomorphous dentition and spatiotemporal isolation, the phylogenetic and biogeographic affinities of Ekgmowechashala have long been debated. Here, we describe the oldest known fossils of Ekgmowechashala from the Brown Siltstone Beds of the Brule Formation, White River Group of western Nebraska. We also describe a new ekgmowechashaline taxon from the Nadu Formation (late Eocene) in the Baise Basin of Guangxi Zhuang Autonomous Region in southern China. Phylogenetic analysis suggests that North American Ekgmowechashala and the new Chinese taxon are sister taxa that are nested within a radiation of southern Asian adapiforms that also includes Gatanthropus, Muangthanhinius, and Bugtilemur. The new Chinese ekgmowechashaline helps fill the considerable disparity in dental morphology between Ekgmowechashala and more primitive ekgmowechashalids known from southern Asia. Our study underscores the fundamental role of southern Asia as a refugium for multiple primate clades during the cooler and drier climatic regime that prevailed after the Eocene-Oligocene transition. The colonization of North America by Ekgmowechashala helps define the beginning of the Arikareean Land Mammal Age and corresponds to an example of the Lazarus effect, whereby a taxon (in this case, the order Primates) reappears suddenly in the fossil record after a lengthy hiatus.

The earliest Asian bats (Mammalia: Chiroptera) address major gaps in bat evolution.

Bats dispersed widely after evolving the capacity for powered flight, and fossil bats are known from the early Eocene of most continents. Until now, however, bats have been conspicuously absent from the early Eocene of mainland Asia. Here, we report two teeth from the Junggar Basin of northern Xinjiang, China belonging to the first known early Eocene bats from Asia, representing arguably the most plesiomorphic bat molars currently recognized. These teeth combine certain bat synapomorphies with primitive traits found in other placental mammals, thereby potentially illuminating dental evolution among stem bats. The Junggar Basin teeth suggest that the dentition of the stem chiropteran family Onychonycteridae is surprisingly derived, although their postcranial anatomy is more primitive than that of any other Eocene bats. Additional comparisons with stem bat families Icaronycteridae and Archaeonycteridae fail to identify unambiguous synapomorphies for the latter taxa, raising the possibility that neither is monophyletic as currently recognized. The presence of highly plesiomorphic bats in the early Eocene of central Asia suggests that this region was an important locus for the earliest, transitional phases of bat evolution, as has been demonstrated for other placental mammal orders including Lagomorpha and Rodentia.

The oldest known primate skeleton and early haplorhine evolution.

Reconstructing the earliest phases of primate evolution has been impeded by gaps in the fossil record, so that disagreements persist regarding the palaeobiology and phylogenetic relationships of the earliest primates. Here we report the discovery of a nearly complete and partly articulated skeleton of a primitive haplorhine primate from the early Eocene of China, about 55 million years ago, the oldest fossil primate of this quality ever recovered. Coupled with detailed morphological examination using propagation phase contrast X-ray synchrotron microtomography, our phylogenetic analysis based on total available evidence indicates that this fossil is the most basal known member of the tarsiiform clade. In addition to providing further support for an early dichotomy between the strepsirrhine and haplorhine clades, this new primate further constrains the age of divergence between tarsiiforms and anthropoids. It also strengthens the hypothesis that the earliest primates were probably diurnal, arboreal and primarily insectivorous mammals the size of modern pygmy mouse lemurs.

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.

Estimating body size in early primates: The case of Archicebus and Teilhardina.

Obtaining accurate estimations of the body mass of fossil primates has always been a subject of interest in paleoanthropology because mass is an important determinant for so many other aspects of biology, ecology, and life history. This paper focuses on the issues involved in attempting to reconstruct the mass of two early Eocene haplorhine primates, Teilhardina and Archicebus, which pose particular problems due to their small size and temporal and phylogenetic distance from extant primates. In addition to a ranking of variables from more to less useful, the effect of using models of varying taxonomic and size compositions is examined. Phylogenetic correction is also applied to the primate database. Our results indicate that the choice of variable is more critical than the choice of model. The more reliable variables are the mediolateral breadth across the femoral condyles and the area of the calcaneocuboid facet of the calcaneus. These variables suggest a body mass of 39 g (range 33-46 g) for Archicebus and 48 g (range 44-56 g) for Teilhardina. The width of the distal femur is found to be the most consistent estimator across models of various composition and techniques. The effect of phylogenetic correction is small but the choice of branch length assumption affects point estimates for the fossils. The majority of variables and models predict the body mass of Archicebus and Teilhardina to be in the range of the smaller extant mouse lemurs, as expected.

Phalangeal morphology of Shanghuang fossil primates.

Here, we describe hundreds of isolated phalanges attributed to middle Eocene fossil primates from the Shanghuang fissure-fillings from southern Jiangsu Province, China. Extending knowledge based on previous descriptions of postcranial material from Shanghuang, this sample of primate finger and toe bones includes proximal phalanges, middle phalanges, and over three hundred nail-bearing distal phalanges. Most of the isolated proximal and middle phalanges fall within the range of small-bodied individuals, suggesting an allocation to the smaller haplorhine primates identified at Shanghuang, including eosimiids. In contrast to the proximal and middle phalanges from Shanghuang, there are a variety of shapes, sizes, and possible taxonomic allocations for the distal phalanges. Two distal phalangeal morphologies are numerically predominant at Shanghuang. The sample of larger bodied specimens is best allocated to the medium-sized adapiform Adapoides while the smaller ones are allocated to eosimiids on the basis of the commonality of dental and tarsal remains of these taxa at Shanghuang. The digit morphology of Adapoides is similar morphologically to that of notharctines and cercamoniines, while eosimiid digit morphology is unlike living anthropoids. Other primate distal phalangeal morphologies at Shanghuang include grooming "claws" as well as specimens attributable to tarsiids, tarsiiforms, the genus Macrotarsius, and a variety of adapiforms. One group of distal phalanges at Shanghuang is morphologically indistinguishable from those of living anthropoids. All of the phalanges suggest long fingers and toes for the fossil primates of Shanghaung, and their digit morphology implies arboreality with well-developed digital flexion and strong, grasping hands and feet.

Distal phalanges of Eosimias and Hoanghonius.

Seven primate distal phalanges have been identified from two middle Eocene fossil localities (Locality 1 and Nanbaotou) in the Yuanqu Basin, China, providing the first evidence of distal phalangeal morphology in Asian Eocene adapiform and eosimiid primates. The bones are best allocated to the basal anthropoid Eosimias centennicus and to hoanghoniine adapiforms. All distal phalangeal specimens display a morphology consistent with nail-bearing fingers and toes. The hallucal distal phalanx of the basal anthropoid Eosimias is more similar to that of primitive tarsiiforms than to crown group anthropoids. The adapiform distal phalanges from Locality 1 are allocated to Hoanghonius stehlini while those from Nanbaotou are tentatively assigned to an indeterminate hoanghoniine because dental remains of adapiforms have yet to be identified from this site. The distal phalangeal anatomy of hoanghoniines differs slightly from that documented for adapines and notharctines. One distal phalanx from Locality 1 shows a second pedal digit "grooming claw" morphology as noted for notharctines by Maiolino et al. (2012) and cercamoniines by Von Koenigswald et al. (2012).

Lufengpithecus inner ear provides evidence of a common locomotor repertoire ancestral to human bipedalism.

Various lines of evidence have been used to infer the origin of human bipedalism, but the paucity of hominoid postcranial fossils and the diversity of inferred locomotor modes have tended to confound the reconstruction of ancestral morphotypes. Examination of the bony labyrinth morphology of the inner ear of extinct and living hominoids provides independent evidence for inferring the evolution of hominoid locomotor patterns. New computed tomography data and morphometric analyses of the Late Miocene ape Lufengpithecus indicate that it and other stem great apes possess labyrinths similar to one another and show that hominoids initially evolved from a positional repertoire that included orthogrady, below-branch forelimb suspension and progression, above-branch bipedalism, climbing, clambering, and leaping (hylobatid-like) to one that comprised above-branch quadrupedalism, below-branch forelimb suspension, vertical climbing, limited leaping, terrestrial quadrupedal running and walking, possibly with knuckle walking, and short bouts of bipedalism (chimpanzee-like). The bony labyrinth morphology of Lufengpithecus indicates that it probably conforms more closely to the last common ancestors of crown hominoids and hominids in its locomotor behavior than do other Miocene hominoids. Human bipedalism evolved from this common archetypal Lufengpithecus-like locomotor repertoire. The low evolutionary rate of semicircular canal morphology suggests that Lufengpithecus experienced a relative stasis in locomotor behavior, probably due to the uplift of the Tibetan Plateau, which created a stable environment in the Miocene of southwestern China.

Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters.

The phylogenetic relationships of notoungulates, an extinct group of predominantly South American herbivores, remain poorly resolved with respect to both other placental mammals and among one another. Most previous phylogenetic analyses of notoungulates have not included characters of the internal cranium, not least because few such features, including the bony labyrinth, have been described for members of the group. Here we describe the inner ears of the notoungulates Altitypotherium chucalensis (Mesotheriidae), Pachyrukhos moyani (Hegetotheriidae) and Cochilius sp. (Interatheriidae) based on reconstructions of bony labyrinths obtained from computed tomography imagery. Comparisons of the bony labyrinths of these taxa with the basally diverging notoungulate Notostylops murinus (Notostylopidae), an isolated petrosal from Itaboraí, Brazil, referred to Notoungulata, and six therian outgroups, yielded an inner ear character matrix of 25 potentially phylogenetically informative characters, 14 of them novel to this study. Two equivocally optimized character states potentially support a pairing of Mesotheriidae and Hegetotheriidae, whereas four others may be diagnostic of Notoungulata. Three additional characters are potentially informative for diagnosing more inclusive clades: one for crown Placentalia; another for a clade containing Kulbeckia, Zalambdalestes, and Placentalia; and a third for Eutheria (crown Placentalia plus stem taxa). Several other characters are apomorphic for at least one notoungulate in our study and are of potential interest for broader taxonomic sampling within Notoungulata to clarify currently enigmatic interrelationships. Measures of the semicircular canals were used to infer agility (e.g. capable of quick movements vs. lethargic movements) of these taxa. Agility scores calculated from these data generally corroborate interpretations based on postcranial remains of these or closely related species. We provide estimates of the low-frequency hearing limits in notoungulates based on the ratio of radii of the apical and basal turns of the cochlea. These limits range from 15 Hz in Notostylops to 149 Hz in Pachyrukhos, values comparable to the Asian elephant (Elephas maximus) and the California sea lion (Zalophus californianus) when hearing in air, respectively.

Species diversity and postcranial anatomy of eocene primates from Shanghuang, China.

The middle Eocene Shanghuang fissure-fillings, located in southern Jiangsu Province in China near the coastal city of Shanghai (Fig. 1), contain a remarkably diverse array of fossil primates that provide a unique window into the complex role played by Asia during early primate evolution.1 Compared to contemporaneous localities in North America or Europe, the ancient primate community sampled at the Shanghuang fissure-fillings is unique in several ways. Although Shanghuang has some typical Eocene primates (Omomyidae and Adapoidea), it also contains the earliest known members of the Tarsiidae and Anthropoidea (Fig. 2), and some new taxa that are not as yet known from elsewhere. It exhibits a large number of primate species, at least 18, most of which are very small (15-500 g), including some of the smallest primates that have ever been recovered.

First skull of Antillothrix bernensis, an extinct relict monkey from the Dominican Republic.

The nearly pristine remains of Antillothrix bernensis, a capuchin-sized (Cebus) extinct platyrrhine from the Dominican Republic, have been found submerged in an underwater cave. This represents the first specimen of an extinct Caribbean primate with diagnostic craniodental and skeletal parts in association, only the second example of a skull from the region, and one of the most complete specimens of a fossil platyrrhine cranium yet discovered. Cranially, it closely resembles living cebines but is more conservative. Dentally, it is less bunodont and more primitive than Cebus, with crowns resembling Saimiri (squirrel monkeys) and one of the oldest definitive cebines, the late Early Miocene Killikaike blakei from Argentina. The tricuspid second molar also resembles the enigmatic marmosets and tamarins, whose origins continue to present a major gap in knowledge of primate evolution. While the femur is oddly short and stout, the ulna, though more robust, compares well with Cebus. As a member of the cebid clade, Antillothrix demonstrates that insular Caribbean monkeys are not monophyletically related and may not be the product of a single colonizing event. Antillothrix bernensis is an intriguing mosaic whose primitive characters are consistent with an early origin, possibly antedating the assembly of the modern primate fauna in greater Amazonia during the La Venta horizon. While most Greater Antillean primate specimens are quite young geologically, this vanished radiation, known from Cuba (Paralouatta) and Jamaica (Xenothrix) as well as Hispaniola, appears to be composed of long-lived lineages like several other mainland clades.

Massive cranium from Harbin in northeastern China establishes a new Middle Pleistocene human lineage.

It has recently become clear that several human lineages coexisted with Homo sapiens during the late Middle and Late Pleistocene. Here, we report an archaic human fossil that throws new light on debates concerning the diversification of the Homo genus and the origin of H. sapiens. The fossil was recovered in Harbin city in northeastern China, with a minimum uranium-series age of 146 ka. This cranium is one of the best preserved Middle Pleistocene human fossils. Its massive size, with a large cranial capacity (∼1,420 mL) falling in the range of modern humans, is combined with a mosaic of primitive and derived characters. It differs from all the other named Homo species by presenting a combination of features, such as long and low cranial vault, a wide and low face, large and almost square orbits, gently curved but massively developed supraorbital torus, flat and low cheekbones with a shallow canine fossa, and a shallow palate with thick alveolar bone supporting very large molars. The excellent preservation of the Harbin cranium advances our understanding of several less-complete late Middle Pleistocene fossils from China, which have been interpreted as local evolutionary intermediates between the earlier species Homo erectus and later H. sapiens. Phylogenetic analyses based on parsimony criteria and Bayesian tip-dating suggest that the Harbin cranium and some other Middle Pleistocene human fossils from China, such as those from Dali and Xiahe, form a third East Asian lineage, which is a part of the sister group of the H. sapiens lineage. Our analyses of such morphologically distinctive archaic human lineages from Asia, Europe, and Africa suggest that the diversification of the Homo genus may have had a much deeper timescale than previously presumed. Sympatric isolation of small populations combined with stochastic long-distance dispersals is the best fitting biogeographical model for interpreting the evolution of the Homo genus.

Geochemical provenancing and direct dating of the Harbin archaic human cranium.

As one of the most complete archaic human fossils, the Harbin cranium provides critical evidence for studying the diversification of the Homo genus and the origin of Homo sapiens. However, the unsystematic recovery of this cranium and a long and confused history since the discovery impede its accurate dating. Here, we carried out a series of geochemical analyses, including non-destructive X-ray fluorescence (XRF), rare earth elements (REE), and the Sr isotopes, to test the reported provenance of the Harbin cranium and get better stratigraphic constraints. The results show that the Harbin cranium has very similar XRF element distribution patterns, REE concentration patterns, and Sr isotopic compositions to those of the Middle Pleistocene-Holocene mammalian and human fossils recently recovered from the Harbin area. The sediments adhered in the nasal cavity of the Harbin cranium have a 87Sr/86Sr ratio of 0.711898, falling in the variation range measured in a core drilled near the Dongjiang Bridge, where the cranium was discovered during its reconstruction. The regional stratigraphic correlations indicate that the Harbin cranium was probably from the upper part of the Upper Huangshan Formation of the Harbin area, which has an optically stimulated luminescence dating constraint between 138 and 309 ka. U-series disequilibrium dating (n = 10) directly on the cranium suggests that the cranium is older than 146 ka. The multiple lines of evidence from our experiments consistently support the theory that the Harbin cranium is from the late Middle Pleistocene of the Harbin area. Our study also shows that geochemical approaches can provide reliable evidence for locating and dating unsystematically recovered human fossils, and potentially can be applied to other human fossils without clear provenance and stratigraphy records.

A new tarkadectine primate from the Eocene of Inner Mongolia, China: phylogenetic and biogeographic implications.

Tarka and Tarkadectes are Middle Eocene mammals known only from the Rocky Mountains region of North America. Previous work has suggested that they are members of the Plagiomenidae, an extinct family often included in the order Dermoptera. Here we describe a new primate, Tarkops mckennai gen. et sp. nov., from the early Middle Eocene Irdinmanha Formation of Inner Mongolia, China. The new taxon is particularly similar to Tarka and Tarkadectes, but it also displays many features observed in omomyids. A phylogenetic analysis based on a data matrix including 59 taxa and 444 dental characters suggests that Tarkops, Tarka and Tarkadectes form a monophyletic group--the Tarkadectinae--that is nested within the omomyid clade. Within Omomyidae, tarkadectines appear to be closely related to Macrotarsius. Dermoptera, including extant and extinct flying lemurs and plagiomenids, is recognized as a clade nesting within the polyphyletic group of plesiadapiforms, therefore supporting the previous suggestion that the relationship between dermopterans and primates is as close as that between plesiadapiforms and primates. The distribution of tarkadectine primates on both sides of the Pacific Ocean basin suggests that palaeoenvironmental conditions appropriate to sustain primates occurred across a vast expanse of Asia and North America during the Middle Eocene.

The bony labyrinth of the early platyrrhine primate Chilecebus.

We document the morphology of the bony labyrinth of Chilecebus carrascoensis, one of the best preserved early platyrrhines known, based on high resolution CT scanning and 3D digital reconstruction. The cochlea is low and conical in form, as in other anthropoids, but has only 2.5 spiral turns. When the allometric relationship with body mass is considered, cochlear size is similar to that in extant primates. The relative size of the semicircular canals, which is well within the range of other primates, indicates that Chilecebus carrascoensis was probably not as agile in its locomotion as other small-bodied platyrrhines such as Leontopithecus rosalia, Saguinus oedipus, and Callithrix jacchus, but it probably was not a suspensory acrobat or a slow climber. The proportion, shape, and orientation of the semicircular canals in Chilecebus carrascoensis also mirror that typically seen in extant primates. However, no single variable can be used for predicting the locomotor pattern in Chilecebus carrascoensis. Based on Principle Component Analysis (PCA) scores we calculated rescaled Euclidean distances for various taxa; primates with similar locomotor patterns tend to share shorter distances. Results for Chilecebus carrascoensis underscore its general resemblance to living quadrupedal primate taxa, but it is not positioned especially near any single living taxon.

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.