Pliocene bats (Chiroptera) from Kanapoi, Turkana Basin, Kenya.

Fossil bats from the Pliocene of Africa are extremely rare, especially in East Africa where meager records have been reported only from two localities in the Omo River Basin Shungura Formation and from a scattering of localities in the Afar Depression, both in Ethiopia. Here we report on a diverse assemblage of bats from Kanapoi in the Turkana Basin that date to approximately 4.19 million years ago. The Kanapoi bat community consists of four different species of fruit bats including a new genus and two new species as well as five species of echolocating bats, the most common of which are two new species of the molossid genus Mops. Additionally, among the echolocating bats, a new species of the emballonurid Saccolaimus is documented at Kanapoi along with an additional Saccolaimus species and a potentially new species of the nycterid Nycteris. Compared to other East African Pliocene bat assemblages, the Kanapoi bat community is unique in preserving molossids and curiously lacks any evidence of cave dwelling bats like rhinolophids or hipposiderids, which are both common at other East African sites. The bats making up the Kanapoi community all typically roost in trees, with some preferring deeper forests and larger trees (molossids), while the others (pteropodids, nycterids and emballonurids) roost in trees near open areas. Living fruit bats that are related to Kanapoi species typically forage for fruits along the margins of forests and in open savannah. The echolocating forms from Kanapoi consist of groups that aerially hawk for insects in open areas between patches of forest and along water courses. The habitats preferred by living relatives of the Kanapoi bats are in agreement with those constructed for Kanapoi based on other lines of evidence.

Using Phylogenomic Data to Explore the Effects of Relaxed Clocks and Calibration Strategies on Divergence Time Estimation: Primates as a Test Case.

Primates have long been a test case for the development of phylogenetic methods for divergence time estimation. Despite a large number of studies, however, the timing of origination of crown Primates relative to the Cretaceous-Paleogene (K-Pg) boundary and the timing of diversification of the main crown groups remain controversial. Here, we analysed a data set of 372 taxa (367 Primates and 5 outgroups, 3.4 million aligned base pairs) that includes nine primate genomes. We systematically explore the effect of different interpretations of fossil calibrations and molecular clock models on primate divergence time estimates. We find that even small differences in the construction of fossil calibrations can have a noticeable impact on estimated divergence times, especially for the oldest nodes in the tree. Notably, choice of molecular rate model (autocorrelated or independently distributed rates) has an especially strong effect on estimated times, with the independent rates model producing considerably more ancient age estimates for the deeper nodes in the phylogeny. We implement thermodynamic integration, combined with Gaussian quadrature, in the program MCMCTree, and use it to calculate Bayes factors for clock models. Bayesian model selection indicates that the autocorrelated rates model fits the primate data substantially better, and we conclude that time estimates under this model should be preferred. We show that for eight core nodes in the phylogeny, uncertainty in time estimates is close to the theoretical limit imposed by fossil uncertainties. Thus, these estimates are unlikely to be improved by collecting additional molecular sequence data. All analyses place the origin of Primates close to the K-Pg boundary, either in the Cretaceous or straddling the boundary into the Palaeogene.

Continuity of mammalian fauna over the last 200,000 y in the Indian subcontinent.

Mammalian extinction worldwide during the Late Pleistocene has been a major focus for Quaternary biochronology and paleoecology. These extinctions have been variably attributed to the impacts of climate change and human interference. However, until relatively recently, research has been largely restricted to the Americas, Europe, and Australasia. We present the oldest Middle-Late Pleistocene stratified and numerically dated faunal succession for the Indian subcontinent from the Billasurgam cave complex. Our data demonstrate continuity of 20 of 21 identified mammalian taxa from at least 100,000 y ago to the present, and in some cases up to 200,000 y ago. Comparison of this fossil record to contemporary faunal ranges indicates some geographical redistribution of mammalian taxa within India. We suggest that, although local extirpations occurred, the majority of taxa survived or adapted to substantial ecological pressures in fragmented habitats. Comparison of the Indian record with faunal records from Southeast and Southwest Asia demonstrates the importance of interconnected mosaic habitats to long-term faunal persistence across the Asian tropics. The data presented here have implications for mammalian conservation in India today, where increasing ecological circumscription may leave certain taxa increasingly endangered in the most densely populated region of the world.

Internal carotid arterial canal size and scaling in Euarchonta: Re-assessing implications for arterial patency and phylogenetic relationships in early fossil primates.

Primate species typically differ from other mammals in having bony canals that enclose the branches of the internal carotid artery (ICA) as they pass through the middle ear. The presence and relative size of these canals varies among major primate clades. As a result, differences in the anatomy of the canals for the promontorial and stapedial branches of the ICA have been cited as evidence of either haplorhine or strepsirrhine affinities among otherwise enigmatic early fossil euprimates. Here we use micro X-ray computed tomography to compile the largest quantitative dataset on ICA canal sizes. The data suggest greater variation of the ICA canals within some groups than has been previously appreciated. For example, Lepilemur and Avahi differ from most other lemuriforms in having a larger promontorial canal than stapedial canal. Furthermore, various lemurids are intraspecifically variable in relative canal size, with the promontorial canal being larger than the stapedial canal in some individuals but not others. In species where the promontorial artery supplies the brain with blood, the size of the promontorial canal is significantly correlated with endocranial volume (ECV). Among species with alternate routes of encephalic blood supply, the promontorial canal is highly reduced relative to ECV, and correlated with both ECV and cranium size. Ancestral state reconstructions incorporating data from fossils suggest that the last common ancestor of living primates had promontorial and stapedial canals that were similar to each other in size and large relative to ECV. We conclude that the plesiomorphic condition for crown primates is to have a patent promontorial artery supplying the brain and a patent stapedial artery for various non-encephalic structures. This inferred ancestral condition is exhibited by treeshrews and most early fossil euprimates, while extant primates exhibit reduction in one canal or another. The only early fossils deviating from this plesiomorphic condition are Adapis parisiensis with a reduced promontorial canal, and Rooneyia and Mahgarita with reduced stapedial canals.

Inferring echolocation in ancient bats.

Laryngeal echolocation, used by most living bats to form images of their surroundings and to detect and capture flying prey, is considered to be a key innovation for the evolutionary success of bats, and palaeontologists have long sought osteological correlates of echolocation that can be used to infer the behaviour of fossil bats. Veselka et al. argued that the most reliable trait indicating echolocation capabilities in bats is an articulation between the stylohyal bone (part of the hyoid apparatus that supports the throat and larynx) and the tympanic bone, which forms the floor of the middle ear. They examined the oldest and most primitive known bat, Onychonycteris finneyi (early Eocene, USA), and argued that it showed evidence of this stylohyal-tympanic articulation, from which they concluded that O. finneyi may have been capable of echolocation. We disagree with their interpretation of key fossil data and instead argue that O. finneyi was probably not an echolocating bat.

New Oligocene primate from Saudi Arabia and the divergence of apes and Old World monkeys.

It is widely understood that Hominoidea (apes and humans) and Cercopithecoidea (Old World monkeys) have a common ancestry as Catarrhini deeply rooted in Afro-Arabia. The oldest stem Catarrhini in the fossil record are Propliopithecoidea, known from the late Eocene to early Oligocene epochs (roughly 35-30 Myr ago) of Egypt, Oman and possibly Angola. Genome-based estimates for divergence of hominoids and cercopithecoids range into the early Oligocene; however, the mid-to-late Oligocene interval from 30 to 23 Myr ago has yielded little fossil evidence documenting the morphology of the last common ancestor of hominoids and cercopithecoids, the timing of their divergence, or the relationship of early stem and crown catarrhines. Here we describe the partial cranium of a new medium-sized (about 15-20 kg) fossil catarrhine, Saadanius hijazensis, dated to 29-28 Myr ago. Comparative anatomy and cladistic analysis shows that Saadanius is an advanced stem catarrhine close to the base of the hominoid-cercopithecoid clade. Saadanius is important for assessing competing hypotheses about the ancestral morphotype for crown catarrhines, early catarrhine phylogeny and the age of hominoid-cercopithecoid divergence. Saadanius has a tubular ectotympanic but lacks synapomorphies of either group of crown Catarrhini, and we infer that the hominoid-cercopithecoid split happened later, between 29-28 and 24 Myr ago.

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.

Giant lizards occupied herbivorous mammalian ecospace during the Paleogene greenhouse in Southeast Asia.

Mammals dominate modern terrestrial herbivore ecosystems, whereas extant herbivorous reptiles are limited in diversity and body size. The evolution of reptile herbivory and its relationship to mammalian diversification is poorly understood with respect to climate and the roles of predation pressure and competition for food resources. Here, we describe a giant fossil acrodontan lizard recovered with a diverse mammal assemblage from the late middle Eocene Pondaung Formation of Myanmar, which provides a historical test of factors controlling body size in herbivorous squamates. We infer a predominately herbivorous feeding ecology for the new acrodontan based on dental anatomy, phylogenetic relationships and body size. Ranking body masses for Pondaung Formation vertebrates indicates that the lizard occupied a size niche among the larger herbivores and was larger than most carnivorous mammals. Paleotemperature estimates of Pondaung Formation environments based on the body size of the new lizard are approximately 2-5°C higher than modern. These results indicate that competitive exclusion and predation by mammals did not restrict body size evolution in these herbivorous squamates, and elevated temperatures relative to modern climates during the Paleogene greenhouse may have resulted in the evolution of gigantism through elevated poikilothermic metabolic rates and in response to increases in floral productivity.

Climate directly influences Eocene mammal faunal dynamics in North America.

The modern effect of climate on plants and animals is well documented. Some have cautioned against assigning climate a direct role in Cenozoic land mammal faunal changes. We illustrate 3 episodes of significant mammalian reorganization in the Eocene of North America that are considered direct responses to dramatic climatic events. The first episode occurred during the Paleocene-Eocene Thermal Maximum (PETM), beginning the Eocene (55.8 Ma), and earliest Wasatchian North American Land Mammal Age (NALMA). The PETM documents a short (<170 k.y.) global temperature increase of approximately 5 degrees C and a substantial increase in first appearances of mammals traced to climate-induced immigration. A 4-m.y. period of climatic and evolutionary stasis then ensued. The second climate episode, the late early Eocene Climatic Optimum (EECO, 53-50 Ma), is marked by a temperature increase to the highest prolonged Cenozoic ocean temperature and a similarly distinctive continental interior mean annual temperature (MAT) of 23 degrees C. This MAT increase [and of mean annual precipitation (MAP) to 150 cm/y) promoted a major increase in floral diversity and habitat complexity under temporally unique, moist, paratropical conditions. Subsequent climatic deterioration in a third interval, from 50 to 47 Ma, resulted in major faunal diversity loss at both continental and local scales. In this Bridgerian Crash, relative abundance shifted from very diverse, evenly represented, communities to those dominated by the condylarth Hyopsodus. Rather than being "optimum," the EECO began the greatest episode of faunal turnover of the first 15 m.y. of the Cenozoic.

Fossil lemurs from Egypt and Kenya suggest an African origin for Madagascar's aye-aye.

In 1967 G.G. Simpson described three partial mandibles from early Miocene deposits in Kenya that he interpreted as belonging to a new strepsirrhine primate, Propotto. This interpretation was quickly challenged, with the assertion that Propotto was not a primate, but rather a pteropodid fruit bat. The latter interpretation has not been questioned for almost half a century. Here we re-evaluate the affinities of Propotto, drawing upon diverse lines of evidence to establish that this strange mammal is a strepsirrhine primate as originally suggested by Simpson. Moreover, our phylogenetic analyses support the recognition of Propotto, together with late Eocene Plesiopithecus from Egypt, as African stem chiromyiform lemurs that are exclusively related to the extant aye-aye (Daubentonia) from Madagascar. Our results challenge the long-held view that all lemurs are descended from a single ancient colonization of Madagascar, and present an intriguing alternative scenario in which two lemur lineages dispersed from Africa to Madagascar independently, possibly during the later Cenozoic.

A new, large-bodied omnivorous bat (Noctilionoidea: Mystacinidae) reveals lost morphological and ecological diversity since the Miocene in New Zealand.

A new genus and species of fossil bat is described from New Zealand's only pre-Pleistocene Cenozoic terrestrial fauna, the early Miocene St Bathans Fauna of Central Otago, South Island. Bayesian total evidence phylogenetic analysis places this new Southern Hemisphere taxon among the burrowing bats (mystacinids) of New Zealand and Australia, although its lower dentition also resembles Africa's endemic sucker-footed bats (myzopodids). As the first new bat genus to be added to New Zealand's fauna in more than 150 years, it provides new insight into the original diversity of chiropterans in Australasia. It also underscores the significant decline in morphological diversity that has taken place in the highly distinctive, semi-terrestrial bat family Mystacinidae since the Miocene. This bat was relatively large, with an estimated body mass of ~40 g, and its dentition suggests it had an omnivorous diet. Its striking dental autapomorphies, including development of a large hypocone, signal a shift of diet compared with other mystacinids, and may provide evidence of an adaptive radiation in feeding strategy in this group of noctilionoid bats.

33 million year old Myotis (Chiroptera, Vespertilionidae) and the rapid global radiation of modern bats.

The bat genus Myotis is represented by 120+ living species and 40+ extinct species and is found on every continent except Antarctica. The time of divergence of Myotis has been contentious as has the time and place of origin of its encompassing group the Vespertilionidae, the most diverse (450+ species) and widely distributed extant bat family. Fossil Myotis species are common, especially in Europe, beginning in the Miocene but earlier records are poor. Recent study of new specimens from the Belgian early Oligocene locality of Boutersem reveals the presence of a relatively large vespertilionid. Morphological comparison and phylogenetic analysis confirms that the new, large form can be confidently assigned to the genus Myotis, making this record the earliest known for that taxon and extending the temporal range of this extant genus to over 33 million years. This suggests that previously published molecular divergence dates for crown myotines (Myotis) are too young by at least 7 million years. Additionally, examination of first fossil appearance data of 1,011 extant placental mammal genera indicates that only 13 first occurred in the middle to late Paleogene (48 to 33 million years ago) and of these, six represent bats, including Myotis. Paleogene members of both major suborders of Chiroptera (Yangochiroptera and Yinpterochiroptera) include extant genera indicating early establishment of successful and long-term adaptive strategies as bats underwent an explosive radiation near the beginning of the Early Eocene Climatic Optimum in the Old World. A second bat adaptive radiation in the New World began coincident with the Mid-Miocene Climatic Optimum.

The challenges faced by living stock collections in the USA.

Many discoveries in the life sciences have been made using material from living stock collections. These collections provide a uniform and stable supply of living organisms and related materials that enhance the reproducibility of research and minimize the need for repetitive calibration. While collections differ in many ways, they all require expertise in maintaining living organisms and good logistical systems for keeping track of stocks and fulfilling requests for specimens. Here, we review some of the contributions made by living stock collections to research across all branches of the tree of life, and outline the challenges they face.

New Myzopodidae (Chiroptera) from the late Paleogene of Egypt: emended family diagnosis and biogeographic origins of Noctilionoidea.

Myzopodidae is a family of bats today represented by two extant species of the genus Myzopoda that are restricted to the island of Madagascar. These bats possess uniquely derived adhesive pads on their thumbs and ankles that they use for clinging to smooth roosting surfaces. Only one fossil myzopodid has been reported previously, a humerus from Pleistocene deposits at Olduvai Gorge in Tanzania that was tentatively referred to the genus Myzopoda. Here we describe a new genus and two new species of myzopodids based on dental remains from Paleogene deposits in the Fayum Depression in Egypt, and provide an emended diagnosis for the family Myzopodidae. Phasmatonycteris phiomensis n. sp. is represented by four specimens from the early Oligocene Jebel Qatrani Formation and P. butleri n. sp. is known from a single specimen from the late Eocene Birket Qarun Formation. Together these specimens extend the temporal range of Myzopodidae by 36+ million years, and the geographic range by nearly 4000 kilometers. The new myzopodids, along with previously described bats from the Fayum and Australia, suggest that eastern Gondwana played a critical role in the origin and diversification of several bats clades notably including the superfamily Noctilionoidea, the majority of which live in the Neotropics today.

Deep time and the search for anthropoid origins.

Recent fossil discoveries, phylogenetic analyses, revised reconstructions of continental drift, and accumulating molecular evidence have all yielded new information relating to anthropoid origins within the broader context of primate evolution. There is an emerging consensus among molecular studies that four superorders of eutherian mammals can be recognized: Afrotheria, Euarchontoglires (to which primates belong), Laurasiatheria, and Xenarthra. Overall, molecular phylogenies for mammals agree with some statistical analyses of the primate fossil record in indicating an early origin for primates around 85 Ma ago, and the divergence of haplorhines and strepsirrhines at ca. 77 Ma. Such an ancient date for the origin of haplorhines is some 17 Ma prior to the first known possible primate, and some 22 Ma before the earliest fossil evidence of undoubted euprimates. Because anthropoid fossils date back at least to the late Eocene and perhaps to the middle Eocene, and given indications of an early origin for primates, it is unlikely that ancestral anthropoids arose within any other currently known clade of fossil primates (adapiforms, omomyiforms, strepsirrhines, or tarsiiforms). Implications of new molecular, morphological, and biogeographic lines of evidence are explored with respect to the likely time and place of the origin of anthropoids. Four competing, testable hypotheses are reviewed in detail: 1) the Paratethyan hypothesis, 2) the continental Asian hypothesis, 3) the Indo-Madagascar hypothesis, and 4) the African hypothesis. A case is made that current evidence best supports a relatively ancient Gondwanan origin for primates, as well as a Gondwanan (African or Indo-Madagascan) origin for anthropoids at least as old as that of any other currently documented major primate clade. Available fossil evidence at present seems to be most compatible with the African hypothesis, but it is noteworthy that primates are included not in Afrotheria but in Euarchontoglires.

Developmental processes and canine dimorphism in primate evolution.

Understanding the evolutionary history of canine sexual dimorphism is important for interpreting the developmental biology, socioecology and phylogenetic position of primates. All current evidence for extant primates indicates that canine dimorphism is achieved through bimaturism rather than via differences in rates of crown formation time. Using incremental growth lines, we charted the ontogeny of canine formation within species of Eocene Cantius, the earliest known canine-dimorphic primate, to test whether canine dimorphism via bimaturism was developmentally canalized early in primate evolution. Our results show that canine dimorphism in Cantius is achieved primarily through different rates of crown formation in males and females, not bimaturism. This is the first demonstration of rate differences resulting in canine dimorphism in any primate and therefore suggests that canine dimorphism is not developmentally homologous across Primates. The most likely interpretation is that canine dimorphism has been selected for at least twice during the course of primate evolution. The power of this approach is its ability to identify underlying developmental processes behind patterns of morphological similarity, even in long-extinct primate species.

Notharctine primates (Adapiformes) from the early to middle Eocene (Wasatchian-Bridgerian) of Wyoming: transitional species and the origins of Notharctus and Smilodectes.

Notharctine adapiform primates are an abundant element of early (Wasatchian) and middle (Bridgerian) Eocene faunal assemblages from the western interior of North America. Early Eocene notharctine samples are dominated by Cantius with Pelycodus and Copelemur being much rarer and more restricted in their geographic distribution. Cantius is replaced in the middle Eocene by Notharctus and Smilodectes, both of which are common but less widespread, being best known from southwestern Wyoming. The origin of these two middle Eocene taxa has not been well understood, due to a lack of transitional Wasatchian-Bridgerian notharctine faunal samples or because known samples had not been adequately studied. Field work at South Pass in the Greater Green River Basin has produced a relatively large sample of earliest Bridgerian notharctines. Combining this sample with a large, but previously under-studied, sample of notharctines from the latest Wasatchian and earliest Bridgerian in the Wind River Basin has clarified the relationships among Notharctus,Smilodectes, and earlier occurring notharctines. Notharctus first appears in the latest Wasatchian (Wa7), represented by N. venticolus. Phylogenetic analysis supports a Notharctus clade that shares sister taxon status with Cantius nunienus and indicates that Notharctus arose through bifurcation of the lineage containing the last common ancestor of C. nunienus and Notharctus. The origins of Smilodectes are less clear. Phylogenetic analysis supports a clade consisting of Smilodectes and Copelemur, but the origins of both taxa are not established as yet. North American notharctines are typified by relatively low taxonomic diversity, but relatively high abundance and high dental morphological variation (disparity). These attributes are opposite to those of North American omomyids, reflecting differences in ecomorphospace between these two primate radiations.

Omomyid primates (Tarsiiformes) from the Early Middle Eocene at South Pass, Greater Green River Basin, Wyoming.

Recent fieldwork in the Gardnerbuttean (earliest Bridgerian) sediments along the northeastern edge of the Green River Basin at South Pass, Wyoming, has yielded a large and diverse sample of omomyid (tarsiiform) primates. This assemblage includes two species each of Artimonius gen. nov., Washakius, and Omomys, one species of Anaptomorphus, Trogolemur and Uintanius, and a new, primitive species of the rare omomyine genus,Utahia. Utahia is known elsewhere only from its type locality in the Uinta Basin and its phylogenetic position is poorly understood. Utahia carina sp. nov. allows for re-evaluation of the affinities of this genus relative to other omomyines. In most characters, such as a lesser degree of molar trigonid compression, more widely open talonid notches, and a lack of molar talonid crenulation, the new species is more primitive than U. kayi. The dental anatomy of U. carina also indicates that Utahia is morphologically intermediate between washakiins and omomyins, although the balance of anatomical features places Utahia as the sister taxon to a broadly defined "Ourayini" clade. Morphological similarity between U. carina, Loveina zephyri, and primitive Washakius suggests that while the omomyin and washakiin clades may have diverged by the middle Wasatchian, substantial morphological distinctions are first evidenced only in the early Bridgerian. This may be due either to a lack of appropriate faunal samples from older sediments, or, more likely, because ecological circumstances in the early Bridgerian favored omomyine diversification and subsequent replacement of previously occurring taxa. This hypothesis is further supported by the stratigraphic co-occurrence of U. carina, W. izetti, and a primitive variant of W. insignis at South Pass, a marginal area. Basin margins have been hypothesized to provide heterogeneous habitats conducive to the production of evolutionary innovation. Basin margin samples have also been cited as evidence that anaptomorphines were relegated to upland refugia as omomyine taxa began to appear in the later part of the early Eocene. Another possible explanation for the unusual co-occurrence of species at South Pass relates to fluctuating lake levels in the Green River Basin, which intermittently would have made lowland environments inhospitable for arboreal fauna. This would have created a situation whereby species which would normally be allopatric become sympatric at South Pass.