Iyad S. Zalmout

Middle East Respiratory Syndrome Coronavirus Infection in Dromedary Camels in Saudi Arabia

ABSTRACT The Middle East respiratory syndrome (MERS) is proposed to be a zoonotic disease; however, the reservoir and mechanism for transmission of the causative agent, the MERS coronavirus, are unknown. Dromedary camels have been implicated through reports that some victims have been exposed to camels, camels in areas where the disease has emerged have antibodies to the virus, and viral sequences have been recovered from camels in association with outbreaks of the disease among humans. Nonetheless, whether camels mediate transmission to humans is unresolved. Here we provide evidence from a geographic and temporal survey of camels in the Kingdom of Saudi Arabia that MERS coronaviruses have been circulating in camels since at least 1992, are distributed countrywide, and can be phylogenetically classified into clades that correlate with outbreaks of the disease among humans. We found no evidence of infection in domestic sheep or domestic goats. IMPORTANCE This study was undertaken to determine the historical and current prevalence of Middle East respiratory syndrome (MERS) coronavirus infection in dromedary camels and other livestock in the Kingdom of Saudi Arabia, where the index case and the majority of cases of MERS have been reported. This study was undertaken to determine the historical and current prevalence of Middle East respiratory syndrome (MERS) coronavirus infection in dromedary camels and other livestock in the Kingdom of Saudi Arabia, where the index case and the majority of cases of MERS have been reported.

Middle East Respiratory Syndrome Coronavirus Quasispecies That Include Homologues of Human Isolates Revealed through Whole-Genome Analysis and Virus Cultured from Dromedary Camels in Saudi Arabia

ABSTRACT Complete Middle East respiratory syndrome coronavirus (MERS-CoV) genome sequences were obtained from nasal swabs of dromedary camels sampled in the Kingdom of Saudi Arabia through direct analysis of nucleic acid extracts or following virus isolation in cell culture. Consensus dromedary MERS-CoV genome sequences were the same with either template source and identical to published human MERS-CoV sequences. However, in contrast to individual human cases, where only clonal genomic sequences are reported, detailed population analyses revealed the presence of more than one genomic variant in individual dromedaries. If humans are truly infected only with clonal virus populations, we must entertain a model for interspecies transmission of MERS-CoV wherein only specific genotypes are capable of passing bottleneck selection. IMPORTANCE In most cases of Middle East respiratory syndrome (MERS), the route for human infection with the causative agent, MERS coronavirus (MERS-CoV), is unknown. Antibodies to and viral nucleic acids of MERS-CoV have been found in dromedaries, suggesting the possibility that they may serve as a reservoir or vector for human infection. However, neither whole viral genomic sequence nor infectious virus has been isolated from dromedaries or other animals in Saudi Arabia. Here, we report recovery of MERS-CoV from nasal swabs of dromedaries, demonstrate that MERS-CoV whole-genome consensus sequences from dromedaries and humans are indistinguishable, and show that dromedaries can be simultaneously infected with more than one MERS-CoV. Together with data indicating widespread dromedary infection in the Kingdom of Saudi Arabia, these findings support the plausibility of a role for dromedaries in human infection. In most cases of Middle East respiratory syndrome (MERS), the route for human infection with the causative agent, MERS coronavirus (MERS-CoV), is unknown. Antibodies to and viral nucleic acids of MERS-CoV have been found in dromedaries, suggesting the possibility that they may serve as a reservoir or vector for human infection. However, neither whole viral genomic sequence nor infectious virus has been isolated from dromedaries or other animals in Saudi Arabia. Here, we report recovery of MERS-CoV from nasal swabs of dromedaries, demonstrate that MERS-CoV whole-genome consensus sequences from dromedaries and humans are indistinguishable, and show that dromedaries can be simultaneously infected with more than one MERS-CoV. Together with data indicating widespread dromedary infection in the Kingdom of Saudi Arabia, these findings support the plausibility of a role for dromedaries in human infection.

New Protocetid Whale from the Middle Eocene of Pakistan: Birth on Land, Precocial Development, and Sexual Dimorphism

Background Protocetidae are middle Eocene (49–37 Ma) archaeocete predators ancestral to later whales. They are found in marine sedimentary rocks, but retain four legs and were not yet fully aquatic. Protocetids have been interpreted as amphibious, feeding in the sea but returning to land to rest. Methodology/Principal Findings Two adult skeletons of a new 2.6 meter long protocetid, Maiacetus inuus, are described from the early middle Eocene Habib Rahi Formation of Pakistan. M. inuus differs from contemporary archaic whales in having a fused mandibular symphysis, distinctive astragalus bones in the ankle, and a less hind-limb dominated postcranial skeleton. One adult skeleton is female and bears the skull and partial skeleton of a single large near-term fetus. The fetal skeleton is positioned for head-first delivery, which typifies land mammals but not extant whales, evidence that birth took place on land. The fetal skeleton has permanent first molars well mineralized, which indicates precocial development at birth. Precocial development, with attendant size and mobility, were as critical for survival of a neonate at the land-sea interface in the Eocene as they are today. The second adult skeleton is the most complete known for a protocetid. The vertebral column, preserved in articulation, has 7 cervicals, 13 thoracics, 6 lumbars, 4 sacrals, and 21 caudals. All four limbs are preserved with hands and feet. This adult is 12% larger in linear dimensions than the female skeleton, on average, has canine teeth that are 20% larger, and is interpreted as male. Moderate sexual dimorphism indicates limited male-male competition during breeding, which in turn suggests little aggregation of food or shelter in the environment inhabited by protocetids. Conclusions/Significance Discovery of a near-term fetus positioned for head-first delivery provides important evidence that early protocetid whales gave birth on land. This is consistent with skeletal morphology enabling Maiacetus to support its weight on land and corroborates previous ideas that protocetids were amphibious. Specimens this complete are virtual ‘Rosetta stones’ providing insight into functional capabilities and life history of extinct animals that cannot be gained any other way.

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.

Sequence stratigraphic control on preservation of late Eocene whales and other vertebrates at Wadi Al-Hitan, Egypt

Biological and physical factors govern the distribution of fossils, but it is not always clear which is more important. The preservation of late Eocene vertebrates at the UNESCO World Heritage site of Wadi Al-Hitan, Western Desert of Egypt, is controlled primarily by the physical processes responsible for sequence stratigraphic architecture on a siliciclastic shelf. Three types of stratigraphic surface, each characterized by a taxonomically and taphonomically distinct fossil assemblage, yield most of the known vertebrate fossils. Complete, partially articulated whale skeletons, primarily Basilosaurus isis, are abundant in offshore marine flooding surfaces (MFS) in the late transgressive systems tract (TST) of the first Priabonian sequence (TA4.1), where low net sedimentation rates and environmental averaging in offshore environments promoted the accumulation of carcasses on traceable stratigraphic surfaces. Complete, well-articulated whales, primarily Dorudon atrox, are more widely scattered on minor erosion surfaces in rapidly accumulating shoreface sediments of the overlying falling stage systems tract. Fragmented and abraded vertebrate remains are abundant and diverse in a discontinuous conglomerate that marks the first sequence boundary above the base of the Priabonian (Pr-2), which has not been previously recognized in Egypt, but which formed incised valleys with at least 45 m of total relief. Fossils in this variably thick lag conglomerate include skeletal elements reworked by rivers from underlying marine deposits and bones of terrestrial animals living in the fluvial environment. Marginal marine vertebrates, primarily dugongs, occur on shelly marine ravinement surfaces above Pr-2, in the early TST of the second Priabonian sequence. Most vertebrate remains in Wadi Al-Hitan occur in condensed stratigraphic intervals and taxonomic composition changes with sequence position, both important considerations in interpretation of paleobiological patterns.

Evolution of locomotion in Anthropoidea: the semicircular canal evidence

Our understanding of locomotor evolution in anthropoid primates has been limited to those taxa for which good postcranial fossil material and appropriate modern analogues are available. We report the results of an analysis of semicircular canal size variation in 16 fossil anthropoid species dating from the Late Eocene to the Late Miocene, and use these data to reconstruct evolutionary changes in locomotor adaptations in anthropoid primates over the last 35 Ma. Phylogenetically informed regression analyses of semicircular canal size reveal three important aspects of anthropoid locomotor evolution: (i) the earliest anthropoid primates engaged in relatively slow locomotor behaviours, suggesting that this was the basal anthropoid pattern; (ii) platyrrhines from the Miocene of South America were relatively agile compared with earlier anthropoids; and (iii) while the last common ancestor of cercopithecoids and hominoids likely was relatively slow like earlier stem catarrhines, the results suggest that the basal crown catarrhine may have been a relatively agile animal. The latter scenario would indicate that hominoids of the later Miocene secondarily derived their relatively slow locomotor repertoires.

Kinkonychelys, A New Side-Necked Turtle (Pelomedusoides: Bothremydidae) from the Late Cretaceous of Madagascar

Abstract The type specimen of Kinkonychelys rogersi, n. gen. et sp., is the first turtle skull to be described from the pre-Holocene fossil record of Madagascar. This specimen, a nearly complete cranium, along with several referred specimens (a series of maxillae and a partial lower jaw), was recovered from the Maastrichtian Maevarano Formation in the Mahajanga Basin of northwestern Madagascar. A braincase with the diagnostic characters of Kinkonychelys, but differing in the position of the jaw articulation, formation of the foramen nervi facialis, and a number of other characters, was found in the same rock unit and is provisionally identified as belonging to Kinkonychelys sp., a presumed distinct, but closely related species, too incomplete to be diagnosed at present. Kinkonychelys is a bothremydid because it has the diagnostic characters of an exoccipital-quadrate contact and a fully enclosed incisura columellae auris (Gaffney et al., 2006). Kinkonychelys belongs to the tribe Kurmademydini, previously known to include only Sankuchemys and Kurmademys from the Late Cretaceous of India, because it has a deep fossa pterygoidea, a foramen stapediotemporale facing dorsally, a jugal not retracted from the orbit, a deep fossa precolumellaris, and a large, wide antrum postoticum. Kinkonychelys rogersi and Kinkonychelys sp. both possess a unique form of the overlapping fossa pterygoidea. A cladistic analysis of Kinkonychelys reveals that it is nested within the tribe Kurmademydini of Gaffney et al. (2006) and is related to the other taxa in the tribe as follows: (Sankuchemys (Kinkonychelys+Kurmademys)). The discovery of a Malagasy bothremydid of Maastrichtian age that is nested within the Indian members of the Kurmademydini supports the hypothesis of a connection between Madagascar and the Indian subcontinent that persisted into the late stages of the Late Cretaceous.

Morphology and Function of the Vertebral Column in Remingtonocetus domandaensis (Mammalia, Cetacea) from the Middle Eocene Domanda Formation of Pakistan

The archaeocete family Remingtonocetidae is a group of early cetaceans known from the Eocene of India and Pakistan. Previous studies of remingtonocetids focused primarily on cranial anatomy due to a paucity of well-preserved postcranial material. Here we describe the morphology of the known vertebral column in Remingtonocetus domandaensis based largely on a single well-preserved partial skeleton recovered from the upper Domanda Formation of Pakistan. The specimen preserves most of the precaudal vertebral column in articulation and includes seven complete cervical vertebrae, ten partial to complete thoracic vertebrae, six complete lumbar vertebrae, and the first three sacral vertebrae. Cervical centra are long and possess robust, imbricating transverse processes that stabilized the head and neck. Lumbar vertebrae allowed for limited flexibility and probably served primarily to stabilize the lumbar column during forceful retraction of the hind limbs. Vertebral evidence, taken together with pelvic and femoral morphology, is most consistent with interpretation of Remingtonocetus domandaensis as an animal that swam primarily by powerful movement of its hind limbs rather than dorsoventral undulation of its body axis.

Eotheroides lambondrano, New Middle Eocene Seacow (Mammalia, Sirenia) from the Mahajanga Basin, Northwestern Madagascar

ABSTRACT The first diagnostic sirenian material from Madagascar and, more broadly, the first diagnostic pre-Pleistocene Cenozoic mammal material recovered from the island is reported. Eotheroides lambondrano is a new species of sirenian collected from middle Eocene nearshore marine deposits in the Mahajanga Basin of northwestern Madagascar. The recovered material consists of a nearly complete adult skull (including the first complete rostrum known for Eotheroides) and several portions of pachyosteosclerotic ribs. Diagnostic features of E. lambondrano include: primitive upper dental formula of 3.1.5.3, relatively large occlusal area of M2 and M3, long and narrow nasals, weak rostral deflection compared to other Eocene Dugongidae, well developed supraorbital processes, short infraorbital canal, anteroposteriorly short zygomatic-orbital bridge of maxilla, and a palate that is narrow anteriorly, creating a strongly bellshaped maxillary dental arcade. The cranium of E. lambondrano is similar to that of E. aegyptiacum from the middle Eocene of Egypt in aspects of both morphology and size but the upper molars of E. lambondrano are considerably longer and wider and it has longer, narrower nasals. The age and relatively primitive morphology of E. lambondrano suggests that it may represent the ancestral form from which more northerly species were derived.

PRIABONIAN BASILOSAURUS ISIS (CETACEA) FROM THE WADI ESH-SHALLALA FORMATION: FIRST MARINE MAMMAL FROM THE EOCENE OF JORDAN

FIGURE 1. Map of the Hashemite Kingdom of Jordan showing location of Qa’ Faydat ad Dahikiya in the Eastern Desert of Jordan (on border with Saudi Arabia), with a detailed geological map of Qa’ Faydat ad Dahikiya (modified from Rabba, 1998) and the Basilosaurus locality within this. In 1998 paleontologists at Yarmouk University (Irbid) initiated a field survey and search for fossil vertebrates in the Eastern Desert of the Hashemite Kingdom of Jordan. One promising site, in the Wadi EshShallala Formation of Qa’ Faydat ad Dahikiya, yielded some 20 identifiable elasmobranch teeth of Priabonian age (Mustafa and Zalmout, 1999) and a glauconitic mass containing bone. When cleaned, the bone was recognized as a caudal vertebra of a large marine mammal. Comparison with archaeocete specimens from the late Eocene of Egypt shows that it is a 14th caudal vertebra of Basilosaurus isis. The specimen is important in corroborating the Priabonian age of the upper Wadi Esh-Shallala Formation, it is the first record of marine mammals in the Eocene of Jordan, and it offers promise for discovery of additional specimens in the future. Institutional Abbreviations—YUPC, paleontological collections of the Department of Earth and Environmental Sciences, Yarmouk University, Irbid; UM, Museum of Paleontology, University of Michigan, Ann Arbor; USNM, U.S. National Museum, Smithsonian Institution, Washington.