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Yingying Li,
Jean-Bosco Ndjango,
Gerald H Learn,
Miguel A Ramirez,
Brandon F Keele,
Frederic Bibollet-Ruche,
Weimin Liu,
Juliet L Easlick,
Julie M Decker,
Rebecca S Rudicell, [......],
Vernon Reynolds,
Martin N Muller,
Rebecca L Chancellor,
Aaron S Rundus,
Nicole Simmons, Michael Worobey,
George M Shaw,
Martine Peeters,
Paul M Sharp,
Beatrice H Hahn
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ABSTRACT: Chimpanzees in west central Africa (Pan troglodytes troglodytes) are endemically infected with simian immunodeficiency viruses (SIVcpzPtt) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa (Pan troglodytes schweinfurthii) are also infected with SIVcpz; however, their viruses (SIVcpzPts) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos (Pan paniscus) in the DRC, a species not previously tested for SIV in the wild. Fecal samples (n = 3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km(2). In this region, SIVcpzPts was common and widespread, with seven field sites exhibiting infection rates of 30% or greater. The overall prevalence of SIVcpzPts infection was 13.4% (95% confidence interval, 10.7% to 16.5%). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpzPts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpzPts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.
Journal of Virology 07/2012; 86(19):10776-91. · 5.40 Impact Factor
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ABSTRACT: Little is known about the origin and long-term evolutionary mode of retroviruses. Retroviruses can integrate into their hosts' genomes, providing a molecular fossil record for studying their deep history. Here we report the discovery of an endogenous foamy virus-like element, which we designate 'coelacanth endogenous foamy-like virus' (CoeEFV), within the genome of the coelacanth (Latimeria chalumnae). Phylogenetic analyses place CoeEFV basal to all known foamy viruses, strongly suggesting an ancient ocean origin of this major retroviral lineage, which had previously been known to infect only land mammals. The discovery of CoeEFV reveals the presence of foamy-like viruses in species outside the Mammalia. We show that foamy-like viruses have likely codiverged with their vertebrate hosts for more than 407 million years and underwent an evolutionary transition from water to land with their vertebrate hosts. These findings suggest an ancient marine origin of retroviruses and have important implications in understanding foamy virus biology.
PLoS Pathogens 06/2012; 8(6):e1002790. · 9.13 Impact Factor
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ABSTRACT: We report the discovery and analysis of an endogenous foamy virus (PSFVaye) within the genome of the aye-aye (Daubentonia madagascariensis), a strepsirrhine primate from Madagascar. Phylogenetic analyses indicate that PSFVaye is divergent from all known simian foamy viruses, suggesting an association between foamy viruses and primates since the haplorrhine-strepsirrhine split. The discovery of PSFVaye indicates that primate foamy virus might be more broadly distributed than previously thought.
Journal of Virology 05/2012; 86(14):7696-8. · 5.40 Impact Factor
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ABSTRACT: Endogenous retroviruses provide molecular fossils for studying the ancient evolutionary history of retroviruses. Here, we report our independent discovery and analysis of endogenous lentiviral insertions (Mustelidae endogenous lentivirus [MELV]) within the genomes of weasel family (Mustelidae). Genome-scale screening identified MELV elements in the domestic ferret (Mustela putorius furo) genome (MELVmpf). MELVmpf exhibits a typical lentiviral genomic organization. Phylogenetic analyses position MELVmpf basal to either primate lentiviruses or feline immunodeficiency virus. Moreover, we verified the presence of MELV insertions in the genomes of several species of the Lutrinae and Mustelinae subfamilies but not the Martinae subfamily, suggesting that the invasion of MELV into the Mustelidae genomes likely took place between 8.8 and 11.8 Ma. The discovery of MELV in weasel genomes extends the host range of lentiviruses to the Caniformia (order Carnivora) and provides important insights into the prehistoric diversity of lentiviruses.
Molecular Biology and Evolution 04/2012; 29(10):2905-8. · 5.55 Impact Factor
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ABSTRACT: Recombination is an important process that influences biological evolution at many different levels. More and more homologous recombination events have been reported among negative sense RNA viruses recently. While sporadic authentic examples indicate that homologous recombination does occur, recombination seems to be generally rare or even absent in most negative sense RNA viruses, and most of the homologous recombination events reported in the literature were likely generated artificially due to lab contamination or inappropriate bioinformatics methods. Homologous recombination in negative sense RNA viruses should be reported with caution in the future, and only after stringent quality control efforts. Moreover, co-infection experiments should be performed to confirm whether recombination can occur.
Viruses 08/2011; 3(8):1358-73. · 1.50 Impact Factor
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ABSTRACT: Investigations into the evolutionary history of the common chimpanzee, Pan troglodytes, have produced inconsistent results due to differences in the types of molecular data considered, the model assumptions employed, and the quantity and geographical range of samples used. We amplified and sequenced 24 complete P. troglodytes mitochondrial genomes from fecal samples collected at multiple study sites throughout sub-Saharan Africa. Using a "relaxed molecular clock," fossil calibrations, and 12 additional complete primate mitochondrial genomes, we analyzed the pattern and timing of primate diversification in a Bayesian framework. Our results support the recognition of four chimpanzee subspecies. Within P. troglodytes, we report a mean (95% highest posterior density [HPD]) time since most recent common ancestor (tMRCA) of 1.026 (0.811-1.263) Ma for the four proposed subspecies, with two major lineages. One of these lineages (tMRCA = 0.510 [0.387-0.650] Ma) contains P. t. verus (tMRCA = 0.155 [0.101-0.213] Ma) and P. t. ellioti (formerly P. t. vellerosus; tMRCA = 0.157 [0.102-0.215] Ma), both of which are monophyletic. The other major lineage contains P. t. schweinfurthii (tMRCA = 0.111 [0.077-0.146] Ma), a monophyletic clade nested within the P. t. troglodytes lineage (tMRCA = 0.380 [0.296-0.476] Ma). We utilized two analysis techniques that may be of widespread interest. First, we implemented a Yule speciation prior across the entire primate tree with separate coalescent priors on each of the chimpanzee subspecies. The validity of this approach was confirmed by estimates based on more traditional techniques. We also suggest that accurate tMRCA estimates from large computationally difficult sequence alignments may be obtained by implementing our novel method of bootstrapping smaller randomly subsampled alignments.
Molecular Biology and Evolution 01/2011; 28(1):615-23. · 5.55 Impact Factor
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Michael Worobey,
Paul Telfer,
Sandrine Souquière,
Meredith Hunter,
Clint A Coleman,
Michael J Metzger,
Patricia Reed,
Maria Makuwa,
Gail Hearn,
Shaya Honarvar,
Pierre Roques,
Cristian Apetrei,
Mirdad Kazanji,
Preston A Marx
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ABSTRACT: Simian immunodeficiency virus (SIV) lineages have been identified that are endemic to Bioko Island. The time the island formed offers a geological time scale calibration point for dating the most recent common ancestor of SIV. The Bioko viruses cover the whole range of SIV genetic diversity, and each Bioko SIV clade is most closely related to viruses circulating in hosts of the same genus on the African mainland rather than to SIVs of other Bioko species. Our phylogeographic approach establishes that SIV is ancient and at least 32,000 years old. Our conservative calibration point and analyses of gene sequence saturation and dating bias suggest it may be much older.
Science 09/2010; 329(5998):1487. · 31.20 Impact Factor
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ABSTRACT: Multiple factors over the lifetime of an individual, including diet, geography, and physiologic state, will influence the microbial communities within the primate gut. To determine the source of variation in the composition of the microbiota within and among species, we investigated the distal gut microbial communities harbored by great apes, as present in fecal samples recovered within their native ranges. We found that the branching order of host-species phylogenies based on the composition of these microbial communities is completely congruent with the known relationships of the hosts. Although the gut is initially and continuously seeded by bacteria that are acquired from external sources, we establish that over evolutionary timescales, the composition of the gut microbiota among great ape species is phylogenetically conserved and has diverged in a manner consistent with vertical inheritance.
PLoS Biology 01/2010; 8(11):e1000546. · 11.45 Impact Factor
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ABSTRACT: Because a constant rate of DNA sequence evolution cannot be assumed to be ubiquitous, relaxed molecular clock inference models have proven useful when estimating rates and divergence dates. Furthermore, it has been recently suggested that using relaxed molecular clocks may provide superior accuracy and precision in phylogenetic inference compared with traditional time-free methods that do not incorporate a molecular clock. We perform a simulation study to determine if assuming a relaxed molecular clock does indeed improve the quality of phylogenetic inference. We analyze sequence data simulated under various rate distributions using relaxed-clocks, strict-clocks, and time-free Bayesian phylogenetic inference models. Our results indicate that no difference exists in the quality of phylogenetic inference between assuming a relaxed molecular clock and making no assumption about the clock-likeness of sequence evolution. This pattern is likely due to the bias-variance trade-off inherent in this type of phylogenetic inference. We also compared the quality of inference between Bayesian and maximum likelihood time-free inference models and found them to be qualitatively similar.
Systematic Biology 01/2010; 59(1):1-8. · 10.23 Impact Factor
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Gavin J D Smith,
Dhanasekaran Vijaykrishna,
Justin Bahl,
Samantha J Lycett, Michael Worobey,
Oliver G Pybus,
Siu Kit Ma,
Chung Lam Cheung,
Jayna Raghwani,
Samir Bhatt,
J S Malik Peiris,
Yi Guan,
Andrew Rambaut
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ABSTRACT: In March and early April 2009, a new swine-origin influenza A (H1N1) virus (S-OIV) emerged in Mexico and the United States. During the first few weeks of surveillance, the virus spread worldwide to 30 countries (as of May 11) by human-to-human transmission, causing the World Health Organization to raise its pandemic alert to level 5 of 6. This virus has the potential to develop into the first influenza pandemic of the twenty-first century. Here we use evolutionary analysis to estimate the timescale of the origins and the early development of the S-OIV epidemic. We show that it was derived from several viruses circulating in swine, and that the initial transmission to humans occurred several months before recognition of the outbreak. A phylogenetic estimate of the gaps in genetic surveillance indicates a long period of unsampled ancestry before the S-OIV outbreak, suggesting that the reassortment of swine lineages may have occurred years before emergence in humans, and that the multiple genetic ancestry of S-OIV is not indicative of an artificial origin. Furthermore, the unsampled history of the epidemic means that the nature and location of the genetically closest swine viruses reveal little about the immediate origin of the epidemic, despite the fact that we included a panel of closely related and previously unpublished swine influenza isolates. Our results highlight the need for systematic surveillance of influenza in swine, and provide evidence that the mixing of new genetic elements in swine can result in the emergence of viruses with pandemic potential in humans.
Nature 07/2009; 459(7250):1122-5. · 36.28 Impact Factor
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Gavin J. D. Smith,
Dhanasekaran Vijaykrishna,
Justin Bahl,
Samantha J. Lycett, Michael Worobey,
Oliver G. Pybus,
Siu Kit Ma,
Chung Lam Cheung,
Jayna Raghwani,
Samir Bhatt,
J. S. Malik Peiris,
Yi Guan,
Andrew Rambaut
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ABSTRACT: In March and early April 2009, a new swine-origin influenza A (H1N1) virus (S-OIV) emerged in Mexico and the United States
Nature 06/2009; 459(7250):1122-1125. · 36.28 Impact Factor
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ABSTRACT: Great strides have been made in understanding the evolutionary history of simian immunodeficiency virus (SIV) and the zoonoses that gave rise to HIV-1 and HIV-2. What remains unknown is how long these SIVs had been circulating in non-human primates before the transmissions to humans. Here, we use relaxed molecular clock dating techniques to estimate the time of most recent common ancestor for the SIVs infecting chimpanzees and sooty mangabeys, the reservoirs of HIV-1 and HIV-2, respectively. The date of the most recent common ancestor of SIV in chimpanzees is estimated to be 1492 (1266-1685), and the date in sooty mangabeys is estimated to be 1809 (1729-1875). Notably, we demonstrate that SIV sequences sampled from sooty mangabeys possess sufficient clock-like signal to calibrate a molecular clock; despite the differences in host biology and viral dynamics, the rate of evolution of SIV in sooty mangabeys is indistinguishable from that of its human counterpart, HIV-2. We also estimate the ages of the HIV-2 human-to-human transmissible lineages and provide the first age estimate for HIV-1 group N at 1963 (1948-1977). Comparisons between the SIV most recent common ancestor dates and those of the HIV lineages suggest a difference on the order of only hundreds of years. Our results suggest either that SIV is a surprisingly young lentiviral lineage or that SIV and, perhaps, HIV dating estimates are seriously compromised by unaccounted-for biases.
PLoS Computational Biology 06/2009; 5(5):e1000377. · 5.22 Impact Factor
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ABSTRACT: Mucin-like regions contribute to pathogenicity in a variety of negative-stranded RNA viruses. These regions are characterized by a preponderance of O-linked glycosylation. They evolve exceptionally rapidly yet maintain their function as pathogenicity factors. Two hypotheses have been proposed to explain this evolutionary conundrum of phenotypic stability in the face of extreme genetic divergence: strong positive selection and relaxation of purifying selection. We determined the strength and direction of selection codon by codon across genes containing these regions and found that purifying selection is relaxed over the mucin-like regions relative to the genes in which they are found. This suggests that so long as these regions maintain sufficient O-linked glycosylation, they are free to evolve rapidly without loss of function as pathogenicity factors.
Journal of Virology 03/2009; 83(9):4690-4. · 5.40 Impact Factor
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Michael Worobey,
Marlea Gemmel,
Dirk E Teuwen,
Tamara Haselkorn,
Kevin Kunstman,
Michael Bunce,
Jean-Jacques Muyembe,
Jean-Marie M Kabongo,
Raphaël M Kalengayi,
Eric Van Marck,
M Thomas P Gilbert,
Steven M Wolinsky
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ABSTRACT: Human immunodeficiency virus type 1 (HIV-1) sequences that pre-date the recognition of AIDS are critical to defining the time of origin and the timescale of virus evolution. A viral sequence from 1959 (ZR59) is the oldest known HIV-1 infection. Other historically documented sequences, important calibration points to convert evolutionary distance into time, are lacking, however; ZR59 is the only one sampled before 1976. Here we report the amplification and characterization of viral sequences from a Bouin's-fixed paraffin-embedded lymph node biopsy specimen obtained in 1960 from an adult female in Léopoldville, Belgian Congo (now Kinshasa, Democratic Republic of the Congo (DRC)), and we use them to conduct the first comparative evolutionary genetic study of early pre-AIDS epidemic HIV-1 group M viruses. Phylogenetic analyses position this viral sequence (DRC60) closest to the ancestral node of subtype A (excluding A2). Relaxed molecular clock analyses incorporating DRC60 and ZR59 date the most recent common ancestor of the M group to near the beginning of the twentieth century. The sizeable genetic distance between DRC60 and ZR59 directly demonstrates that diversification of HIV-1 in west-central Africa occurred long before the recognized AIDS pandemic. The recovery of viral gene sequences from decades-old paraffin-embedded tissues opens the door to a detailed palaeovirological investigation of the evolutionary history of HIV-1 that is not accessible by other methods.
Nature 11/2008; 455(7213):661-4. · 36.28 Impact Factor
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Weimin Liu, Michael Worobey,
Yingying Li,
Brandon F Keele,
Frederic Bibollet-Ruche,
Yuanyuan Guo,
Paul A Goepfert,
Mario L Santiago,
Jean-Bosco N Ndjango,
Cecile Neel, [......],
Vince Smith,
Koichiro Zamma,
Michael A Huffman,
John C Mitani,
David P Watts,
Martine Peeters,
George M Shaw,
William M Switzer,
Paul M Sharp,
Beatrice H Hahn
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ABSTRACT: Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.
PLoS Pathogens 08/2008; 4(7):e1000097. · 9.13 Impact Factor
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Michael Worobey
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ABSTRACT: Zhang et al. (G. Zhang, D. Shoham, D. Gilichinsky, S. Davydov, J. D. Castello, and S. O. Rogers, J. Virol. 80:12229-12235, 2006) have claimed to have recovered influenza A virus RNA from Siberian lake ice, postulating that ice might represent an important abiotic reservoir for the persistence and reemergence of this medically important pathogen. A rigorous phylogenetic analysis of these influenza A virus hemagglutinin gene sequences, however, indicates that they originated from a laboratory reference strain derived from the earliest human influenza A virus isolate, WS/33. Contrary to Zhang et al.'s assertions that the Siberian "ice viruses" are most closely related either to avian influenza virus or to human influenza virus strains from Asia from the 1960s (Zhang et al., J. Virol. 81:2538 [erratum], 2007), they are clearly contaminants from the WS/33 positive control used in their laboratory. There is thus no credible evidence that environmental ice acts as a biologically relevant reservoir for influenza viruses. Several additional cases with findings that seem at odds with the biology of influenza virus, including modern-looking avian influenza virus RNA sequences from an archival goose specimen collected in 1917 (T. G. Fanning, R. D. Slemons, A. H. Reid, T. A. Janczewski, J. Dean, and J. K. Taubenberger, J. Virol. 76:7860-7862, 2002), can also be explained by laboratory contamination or other experimental errors. Many putative examples of evolutionary stasis in influenza A virus appear to be due to laboratory artifacts.
Journal of Virology 05/2008; 82(7):3769-74. · 5.40 Impact Factor
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Proceedings of the National Academy of Sciences 04/2008; 105(12):E16. · 9.68 Impact Factor
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ABSTRACT: Giardia lamblia (syn. Giardia intestinalis, Giardia duodenalis) is an enteric protozoan parasite with two nuclei, and it might be one of the earliest branching eukaryotes. However, the discovery of at least rudimentary forms of certain features, such as Golgi and mitochondria, has refuted the proposal that its emergence from the eukaryotic lineage predated the development of certain eukaryotic features. The recent recognition of many of the genes known to be required for meiosis in the genome has also cast doubt on the idea that Giardia is primitively asexual, but so far there has been no direct evidence of sexual reproduction in Giardia, and population data have suggested clonal reproduction. We did a multilocus sequence evaluation of the genotype A2 reference strain, JH, and five genotype A2 isolates from a highly endemic area in Peru. Loci from different chromosomes yielded significantly different phylogenetic trees, indicating that they do not share the same evolutionary history; within individual loci, tests for recombination yielded significant statistical support for meiotic recombination. These observations provide genetic data supportive of sexual reproduction in Giardia.
Current Biology 12/2007; 17(22):1984-8. · 9.65 Impact Factor
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ABSTRACT: HIV-1 group M subtype B was the first HIV discovered and is the predominant variant of AIDS virus in most countries outside of sub-Saharan Africa. However, the circumstances of its origin and emergence remain unresolved. Here we propose a geographic sequence and time line for the origin of subtype B and the emergence of pandemic HIV/AIDS out of Africa. Using HIV-1 gene sequences recovered from archival samples from some of the earliest known Haitian AIDS patients, we find that subtype B likely moved from Africa to Haiti in or around 1966 (1962-1970) and then spread there for some years before successfully dispersing elsewhere. A "pandemic" clade, encompassing the vast majority of non-Haitian subtype B infections in the United States and elsewhere around the world, subsequently emerged after a single migration of the virus out of Haiti in or around 1969 (1966-1972). Haiti appears to have the oldest HIV/AIDS epidemic outside sub-Saharan Africa and the most genetically diverse subtype B epidemic, which might present challenges for HIV-1 vaccine design and testing. The emergence of the pandemic variant of subtype B was an important turning point in the history of AIDS, but its spread was likely driven by ecological rather than evolutionary factors. Our results suggest that HIV-1 circulated cryptically in the United States for approximately 12 years before the recognition of AIDS in 1981.
Proceedings of the National Academy of Sciences 12/2007; 104(47):18566-70. · 9.68 Impact Factor
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Andrew S Wilson,
Timothy Taylor,
Maria Constanza Ceruti,
Jose Antonio Chavez,
Johan Reinhard,
Vaughan Grimes,
Wolfram Meier-Augenstein,
Larry Cartmell,
Ben Stern,
Michael P Richards, Michael Worobey,
Ian Barnes,
M Thomas P Gilbert
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ABSTRACT: Four recently discovered frozen child mummies from two of the highest peaks in the south central Andes now yield tantalizing evidence of the preparatory stages leading to Inca ritual killing as represented by the unique capacocha rite. Our interdisciplinary study examined hair from the mummies to obtain detailed genetic and diachronic isotopic information. This approach has allowed us to reconstruct aspects of individual identity and diet, make inferences concerning social background, and gain insight on the hitherto unknown processes by which victims were selected, elevated in social status, prepared for a high-altitude pilgrimage, and killed. Such direct information amplifies, yet also partly contrasts with, Spanish historical accounts.
Proceedings of the National Academy of Sciences 11/2007; 104(42):16456-61. · 9.68 Impact Factor
