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Journal of Virology, January 2009, p. 428-439, Vol. 83, No. 1
0022-538X/09/$08.00+0     doi:10.1128/JVI.01725-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Full-Length Genome Characterization of a Novel Simian Immunodeficiency Virus Lineage (SIVolc) from Olive Colobus (Procolobus verus) and New SIVwrcPbb Strains from Western Red Colobus (Piliocolobus badius badius) from the Taï Forest in Ivory Coast

Florian Liégeois,¹ Bénédicte Lafay,^2, Pierre Formenty,³ Sabrina Locatelli,¹ Valérie Courgnaud,^1, Eric Delaporte,¹ and Martine Peeters^1*

UMR 145, Institut de Recherche pour le Developpement (IRD), and University of Montpellier 1, Montpellier, France,¹ UMR CNRS-IRD 2724, Montpellier, France,² Department of Epidemic and Pandemic Alert and Response, World Health Organization, Geneva, Switzerland³

Received 14 August 2008/ Accepted 3 October 2008

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Simian immunodeficiency viruses (SIVs) are found in an extensive number of African primates and humans continue to be exposed to these viruses by hunting and handling of primate bushmeat. Full-length genome sequences were obtained from SIVs derived from two Colobinae species inhabiting the Taï forest, Ivory Coast, each belonging to a different genus: SIVwrc from western red colobus (Piliocolobus badius badius) (SIVwrcPbb-98CI04 and SIVwrcPbb-97CI14) and SIVolc (SIVolc-97CI12) from olive colobus (Procolobus verus). Phylogenetic analysis showed that western red colobus are the natural hosts of SIVwrc, and SIVolc is also a distinct species-specific lineage, although distantly related to the SIVwrc lineage across the entire length of its genome. Overall, both SIVwrc and SIVolc, are also distantly related to the SIVlho/sun lineage across the whole genome. Similar to the group of SIVs (SIVsyk, SIVdeb, SIVden, SIVgsn, SIVmus, and SIVmon) infecting members of the Cercopithecus genus, SIVs derived from western red and olive colobus, L'Hoest and suntailed monkeys, and SIVmnd-1 from mandrills form a second group of viruses that cluster consistently together in phylogenetic trees. Interestingly, the divergent SIVcol lineage, from mantled guerezas (Colobus guereza) in Cameroon, is also closely related to SIVwrc, SIVolc, and the SIVlho/sun lineage in the 5' part of Pol. Overall, these results suggest an ancestral link between these different lentiviruses and highlight once more the complexity of the natural history and evolution of primate lentiviruses.

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Simian immunodeficiency viruses (SIVs) are primate lentiviruses that infect an extensive number of wild African primate species. To date, serological and/or molecular evidence for SIV infections have been reported in at least 40 African nonhuman primate species (4-6, 8-12, 15, 16, 19, 22, 23, 29, 31, 33, 37-39, 50, 56, 58, 59). It is now well established that SIVs from chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in West central Africa and from sooty mangabeys (Cercocebus atys) in West Africa are the progenitors of human immunodeficiency virus type 1 (HIV-1) and HIV-2, respectively, the etiologic agents for AIDS (18, 24, 26, 39, 58). These viruses have crossed the species barriers on multiple occasions and generated different groups of HIV-1 (M, N, and O) and HIV-2 (A to H) (21).

Although SIVs are called immunodeficiency viruses by analogy to HIV, they do not induce, with a few exceptions only (30, 36, 55), AIDS-like disease in their natural hosts. This suggests that they have been associated to, and evolved with, their hosts over an extended period of time. Each primate species is generally infected with a species-specific virus, i.e., multiple strains from the same host species form a monophyletic clade. This was used to establish the SIV nomenclature that names the various SIVs by adding a three letters code of their common name indicating the primate species of origin (e.g., SIVcpz from chimpanzee, SIVsmm from sooty mangabey). When different subspecies of the same species are infected, the name of the subspecies is added to the virus designation, e.g., SIVcpzPtt and SIVcpzPts to differentiate between the two chimpanzee subspecies, P. troglodytes troglodytes and P. troglodytes schweinfurthii, respectively. In some cases, closely related monkey species harbor also closely related SIVs, suggesting that some of these viruses may have coevolved with their hosts for an extended period of time, e.g., L'Hoest and suntailed monkeys from the lhoesti superspecies, and the four species of African green monkeys (genus Chlorocebus) (2, 4, 7, 22, 57, 61). However, there are also numerous examples of cross-species transmission and recombination, e.g., SIVmnd-2 from mandrills, SIVdrl from drill, SIVagm.sab from sabaeus or even SIVcpz from chimpanzees (3, 8, 25, 43, 46). Interestingly, a single primate species can also be infected by two different SIVs. For example, mandrills from central and southern Gabon are infected with SIVmnd-1, whereas those living in northern Gabon and in south Cameroon are infected with SIVmnd-2 (46, 49). Moreover, it was also recently shown that monkeys living on a small geographic area can be infected by two cocirculating SIV variants, e.g., SIVmus-1 and SIVmus-2 in mustached monkeys from Cameroon (1). These observations indicate that both cross-species transmission and coinfection with highly divergent lentiviral strains are possible and that the evolutionary history of primate lentiviruses has been driven by these successive events over an extended period of time.

To date, with the exception of SIVcpz from chimpanzees and the recently discovered SIVgor from west-central gorillas, all nonhuman primate lentiviruses have been isolated from African Old World monkeys (Cercopithecidae), which are subdivided into two distinct subfamilies, Colobinae and Cercopithecinae (20). Colobinae are further separated into African and Asian groups and African colobids are represented by three genera: Colobus, Piliocolobus, and Procolobus (20). Their habitats range over the scattered forested parts of Africa, except for the olive colobus (Procolobus verus), which is confined to a limited area of the tropical forest relicts in West Africa only. SIVs have been documented in a very limited number of colobids only, however, from at least one species of each of the three African colobid genera, i.e., SIVcol from black and white colobus (Colobus guereza) in Cameroon SIVwrc and SIVolc from Western red colobus (Piliocolobus badius) and olive colobus (Procolobus verus), respectively, from West Africa (9, 10, 31). Only SIVcol and SIVwrcPbt, from the Western red colobus subspecies (Piliocolobus badius temminckii) in The Gambia, have been fully characterized. To date, SIVcol represents the most divergent SIV from all known primate lentiviruses. SIVwrcPbt is a species-specific SIV lineage, although distantly related to the SIVlho and SIVsun lineages across its entire genome (10, 31).

The Piliocolobus badius species in West Africa is subdivided into three geographically isolated subspecies: P. badius badius, P. badius waldroni (nearly extinct today) (35), and P. badius temminckii. Partial pol and env sequences of SIVwrcPbb isolated from Western red colobus (P. badius badius) and SIVolc from olive colobus in the Taï forest, Ivory Coast, have been previously described (9, 32). Phylogenetic analyses of these fragments, including the recently described SIVwrcPbt (31), suggest that both SIVwrcPbb and SIVwrcPbt from geographically separate subspecies formed a species-specific monophyletic cluster named SIVwrc lineage (31) and that SIVolc potentially represents a new SIV species-specific lineage (9). To document further the evolutionary history and relationships of SIVs from primates from the Colobinae family, we describe here new full-length genomes from two SIVwrcPbb and one SIVolc, from the Taï forest in Ivory Coast.

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Primate specimens and serologic testing. Between 1997 and 2000, blood and tissue samples (kidney, spleen, lung, liver, and lymph node) from nonhuman primate carcasses found on forest floor were sampled in the Taï national park by sanitary surveillance patrols or by primatologists working in the Taï National Park following an Ebola virus outbreak among chimpanzees as previously described (9). This park, situated in south western Ivory Coast, is the largest remaining area of primary forest in West Africa (Fig. 1). Whole-blood and tissue samples from two wild red colobus (98CI04 97CI14) and one wild olive colobus (97CI12) were available for the present study. The western red colobus samples, 98CI04 and 97CI14, were derived from an adult male of 10 kg and a very old female of 8.5 kg, respectively. The latter died subsequent to a fall from a tree. The olive colobus, 97CI12, was a very old adult female (4.1 kg) killed by an eagle. These animals had previously been shown to be SIV-positive by the presence of cross-reacting antibodies with HIV antigens using Inno-Lia HIV confirmation test and by partial pol sequencing (9). Samples were first stored in liquid nitrogen and later kept at –70°C. The identification of the monkeys was done in the field and confirmed by analysis of the skulls.

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FIG. 1. Location of the Taï National Park in Ivory Coast where the samples were collected (a) and ranges occupied by the different Piliocolobus species and subspecies (gray) and Procolobus species (dark gray) in Africa (b).

PCR amplification and sequencing of SIVwrc and SIVolc full-length genomes. For all samples, total DNA was extracted from whole blood and lymph nodes by using the Qiampblood and Qiamptissue kit, and RNA was extracted from plasma for sample 98CI04 by using the QIAampViral RNA minikit according to the manufacturer's instructions (Qiagen SA, Courtaboeuf, France). For the three samples (98CI04, 97CI14, and 97CI12) a small pol fragment (650 bp) was initially amplified with a set of degenerate consensus primers as previously described (8).

Similarly as for previous reports on full-length characterization of new SIVs (1, 6, 29, 31), complete SIVwrcPbb-98CI04, SIVwrcPbb-97CI14, and SIVolc-97CI12 genomes were obtained by amplification of overlapping PCR fragments and unintegrated circular DNA using combinations of specific SIVwrc and SIVolc primers, as well as degenerate consensus SIV primers. The primers used are shown in Table 1. For sample 98CI04, specific pol primers were designed (Pol0498S1 and Pol0498S2) and reverse transcription-PCR, followed by a seminested PCR, was performed to amplify a 3,000-bp fragment spanning the end of pol, accessory genes, and the beginning of env with a combination of specific and degenerate primers: Pol0498S1/SIV-ER1 for the first round and Pol0498S2/SIV-ER1 for the second round. New specific env primers were then designed (0498ENVS1 and 0498ENVS2), and a seminested PCR was performed with SIVnef-as as the reverse primer to obtain a PCR fragment (1,300 bp) spanning the end of env and the first half of nef. On the basis of the relationship observed between SIVwrcPbb-98CI04 and viruses from the SIVlho lineage in the env phylogeny, consensus primers were designed (ENVF2LHO and ENVR2LHO). For sample 97CI14, a similar PCR amplification strategy was applied for the amplification of the 3' end of pol up to the first half part of nef. Briefly, we performed a nested and seminested PCR with generic SIVwrc pol primers and modified SIV-ER1 primer (SIVenvR) for the first round and ENVF2LHO/ENVR2LHO, followed by WRCenvS2/SIVenvR and PolwrcolF2/WRCenvR1, for the second round. We then performed a seminested PCR with new env-specific primers (1497EnvS4 and 1497EnvS5) and generic nef antisense primer (SIVnef-as). We defined new SIVwrc generic primers for env and carried out PCR amplifications from unintegrated circular DNAs for both samples (98CI04 and 97CI14) using PolwrcolR1/EnvwrcolF1 for the first round, followed by PolwrcolR2/ENVwrcolF2 for the second round. For sample 97CI12, we amplified a 756-bp pol PCR fragment using generic SIVwrc pol primers as previously described (32) and designed new SIVolc-specific pol forward and reverse primers. We then performed nested PCRs spanning the 3' end of pol, the accessory genes, and the 5' beginning of env with specific pol primers and modified env primers (POLF1-1297/SIVenvR for the first round and POLF2-1297/ENVR1-1297 and ENVLHOF2/ENVLHOR2 for the second rounds). In parallel to these PCRs, we amplified a region spanning the second half of gag up to the end of pol using generic and specific primers (SPBS/1297-POLR1 for the first round, followed by SIVgagS/1297-POLR4 and 1297gagF1/1297PolR2 for the second rounds). We then designed new gag- and env-specific primers and amplified unintegrated circular DNA.

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TABLE 1. Primers used to amplify full-length genomes of SIVwrcPbb-98CI04, SIVwrcPbb-97CI14, and SIVolc-97CI12

Reverse transcription-PCR and PCR amplifications were performed by using Expand reverse transcriptase and the Long Expand PCR kit, respectively (Roche Applied Science, Indianapolis, IN) according to the manufacturer's instructions. Each amplification reaction included a manual hot-start, followed by 35 to 40 cycles. Annealing temperatures were set according to the primer melting temperatures, and extension times varied depending on the sizes of the expected fragment and were typically set at 1 min/kb. PCR products were agarose gel purified and directly sequenced by using cycle sequencing and dye terminator methodologies (ABI Prism BigDye terminator cycle sequencing ready reaction kit with AmpliTaq FS DNA polymerase [PE Biosystems, Warrington, England]) on an automated capillary sequencer (ABI 3130XL; Applied Biosystems). To reconstitute the full-length genome sequence, overlapping sequences were assembled into contiguous sequences by using SeqMan DNAStar software (Lasergene; DNAStar, Inc., Madison, WI).

Sequence similarity plots. Nucleotide and protein sequences were aligned by using MEGA3 and CLUSTALX 1.8 (28, 52), with minor manual adjustments. Sites that could not be unambiguously aligned were excluded. Proteome sequences were generated by joining deduced Gag, Pol, Env, and Nef amino acid sequences; the carboxy-terminal Gag and Env amino acid sequences that overlapped with Pol and Nef amino acid sequences respectively, were excluded. The predicted protein sequences encoded by SIVwrcPbb and SIVolc were compared to representatives of known HIV/SIV lineages. In order to study whether the newly characterized SIVwrcPbb and SIVolc sequences were recombinant with any of the other SIV lineages, similarity plot analysis was performed with the SIMPLOT package version 2.5 (41) using a sliding window of 200 amino acids (aa) moved in steps of 20 aa.

Phylogenetic analyses. Amino acid sequence regions used for phylogeny reconstruction were defined on the basis of the simplot results and were as follow: Gag (390 aa), Pol1 (279aa), Pol2 (286 aa), Pol3 (355 aa), and Env (560 aa). Phylogenies were inferred by the Bayesian method implemented in MrBayes v3.1 (64) and run for 3, 5, and 6 million generations for Gag, Pol (Pol1, Pol2, and Pol3), and Env proteomes, respectively, with a 10% burn-in. The mixed model in MrBayes indicated that the rtRET model of amino acid change (14) was most appropriate; this model was thus used with gamma distribution rates across sites (63). Parameters were examined with the Tracer program (Evolutionary Biology Group, Oxford University, Oxford, United Kingdom; http://evolve.zoo.ox.ac.uk/software.html).

RNA Secondary structure predictions. The TAR RNA secondary structure was predicted and drawn by using the GenQuest DNAStar package (Lasergene; DNAStar).

Nucleotide sequence accession numbers. The complete sequences have been deposited to the GenBank under the following numbers: SIVwrcPbb-04CI98 (AM713177), SIVwrcPbb-14CI97 (AM745105), and SIVolc-12CI97 (FM165200, FM165201, and FM165202).

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Genomic organization and functional motifs of SIVwrcPbb and SIVolc. SIVwrcPbb and SIVolc full-length genomes were compared to other primate lentiviruses and showed the expected reading frames for gag, pol, vif, vpr, tat, rev, env, and nef and did not encode for a vpu or vpx analogue. The SIVwrcPbb and SIVolc long terminal repeats (LTRs) contain all of the characteristic features of other primate lentivirus LTRs, including TATA, NF-B sites, and potential SP-1 regions. The secondary structure prediction of SIVwrcPbb TAR showed an unusual organization with a double stem-loop structure consisting of a three nucleotides (GCC) and a single-nucleotide bulge (U) and 7- and 6-bp stems with a 5-bp identical terminal loop with the sequence 5'-CUGGU-3'. Despite some differences, this TAR element is quite similar to the one previously described for SIVwrcPbt from a western red colobus of the P. badius temminckii subspecies in The Gambia (31), which reinforces the common origin of these viruses. In turn, SIVolc has a specific and typical predicted secondary structure of TAR element with two stem-loops consisting of two identical nucleotide bulges (UU) and two 6-bp stems with a 6-bp terminal loop with the sequences 5'-CUGAGU-3' and 5'-CUGGGU-3', respectively.

Like all other known primate lentiviruses, SIVwrcPbb and SIVolc contain 18 cysteine residues conserved across the gp120 envelope glycoprotein surface subunit. Interestingly, the additional cysteine residues described in the SIVlho/sun lineage, SIVdrl/mnd-2 and SIVwrcPbt, are also conserved in both SIVwrcPbb and SIVolc. Finally, two different binding sites known to be critical for primate lentivirus budding have been identified in SIV Gag p6 protein sequences: PT/SAP and YPXL (17, 34, 40, 48, 60). With the exception of SIVdeb and SIVden, both motifs (PT/SAP and YPXL) are found in Cercopithecus and Miopithecus SIV lineages (6, 12, 29) and have been proposed to constitute a specific signature for the Cercopithecus SIV lineage (6). Although both motifs are present in SIVwrcPbt (31), the YPXL motif is absent in SIVwrcPbb and is replaced by a WPXL motif. In contrast, an YPXL motif is present in the SIVolc, thereby increasing the number of non-Cercopithecus SIVs with both PT/SAP and YPXL motifs.

Sequence similarity analyses. In order to compare the new full-length SIVwrcPbb and SIVolc sequences to previously characterized SIV strains, we performed similarity plot analyses on concatenated proteomes, including Gag, Pol, Env, and Nef (Fig. 2 and 3). The accessory genes region, including Vif, was omitted from the alignment due to high sequence heterogeneity and low signal information. Figures 2a and 3a show that, depending on the parts of the genome studied, the new SIVwrcPbb and SIVolc lineages are most closely related to SIVwrcPbt, SIVlho, SIVsun, SIVmnd-2, SIVdrl, and SIVcol. For clarity, representatives of the SIV lineages most relevant to our study are shown separately in Fig. 2b and 3b.

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FIG. 2. Similarity plots of concatened Gag, Pol, Env, and Nef protein sequences showing similarities between SIVwrcPbb versus other SIVs representative for the different SIV lineages, obtained with a sliding window of 200 aa moved in steps of 20 aa. SIV lineages with a high interest for our study, namely, SIVwrcPbt, SIVlho, SIVsun, SIVdrl, SIVmnd-2, and SIVcol, are shown in the large-scale window (b), whereas the comparison with all of the representative SIV strains known is represented in the smallest window (a). The vertical axis shows the percentage of similarities, and the horizontal axis shows the amino acid positions.

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FIG. 3. Similarity plots of concatened Gag, Pol, Env, and Nef protein sequences showing similarities between SIVolc versus other SIVs representative for the different SIV lineages, obtained with a sliding window of 200 aa moved in steps of 20 aa. SIV lineages with a high interest for our study, namely, SIVwrc, SIVlho, SIVsun, SIVdrl, SIVmnd-2, and SIVcol, are shown in the large-scale window (b), whereas the comparison with all of the representative SIV strains known is presented in the smallest window (a). The vertical axis shows the percentage of similarities, and the horizontal axis shows the amino acid positions.

Figure 2b depicts in more detail similarities between SIVwrcPbb-98CI04 and SIVwrcPbb-97CI14, as well as with the other representative relevant SIV lineages. The two SIVwrcPbb strains were quite similar to one another and shared 81 to 95% amino acid identity depending on the gene analyzed, as shown in Table 2. Across their entire genomes, SIVwrcPbb were also closely linked to the recently characterized SIVwrcPbt from the geographically separated temminckii subspecies in the Gambia (31). As described for SIVwrcPbt, SIVwrcPbb strains were thus also more closely related to the SIVlho/sun lineage than to any other SIV, particularly in two parts of their proteomes corresponding to the 5' part of Pol and to the entire Env.

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TABLE 2. Percent amino acid identity between SIVwrcPbb (04CI98 and 14CI97), SIVolc (12CI97), and SIV strains representative of other SIV lineages in the three major fragments, Gag, Pol, and Env

Figure 3b shows similarities between SIVolc from olive colobus and the other representative SIV strains. SIVolc is related to SIVwrc across almost the entire genome, and SIVolc is thus also related to the SIVlho lineage in the regions corresponding to the 5' part of Pol and over the entire Env. In addition, the similarity plots show also that SIVcol is closer to the SIVwrc, SIVolc, and SIVlho lineages than to SIVs from other monkey species in the N-terminal part of Pol. In the Pol protein, three different patterns are observed: in the N-terminal part as well as in the C-terminal part of the Pol region, SIVolc seemed to be more closely related to SIVwrc strains, whereas in the middle part of the Pol region the SIV relationships were unclear. Overall, these results suggest a complex evolutionary history between ancestral SIVs in the Colobinae subfamily and strains from the SIVlho/sun lineage, possibly driven by cross-species transmission and recombination events over an extended period of time.

Phylogenetic analyses of full-length SIVwrcPbb and SIVolc genomes. The different phylogenetic trees show that SIVwrcPbb and SIVolc are each distinct species-specific SIV lineages but distantly related across their entire genomes. SIVwrcPbb forms a monophyletic species-specific lineage with the recently described SIVwrcPbt strain (31) in the phylogenies obtained with each of the three major proteins (Fig. 4), as well as in the accessory proteins (data not shown). For more detailed phylogenetic analysis, the Pol protein has been subdivided into three fragments, according to the observations of the similarity plot analysis of SIVolc versus the other SIVs.

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FIG. 4. Phylogenetic relationships between SIVwrcPbb and SIVolc with other representative SIV lineages in Gag (a), Pol (b, c, and d), and Env (e) genes. Phylogenies were inferred by using the Bayesian method. Stars at node represent posterior probabilities. Only those at 91% are shown. Scale bars indicate substitutions per site.

For each protein analyzed, both SIVwrc and SIVolc lineages clustered together, although distantly related to each other, but also distantly related to the SIVlho lineage that includes SIVlho and SIVsun from L'Hoest and sun-tailed monkeys and SIVmnd-1 from mandrills. In Gag (Fig. 4a), the highest level of divergence is observed between the above-mentioned SIV lineages. Interestingly, in all phylogenies except in Pol2, SIVolc conserves a basal position compared to SIVwrc. In the Gag and Pol1 trees (Fig. 4a and b), SIVcol from Colobus guereza clustered also with SIVwrc, SIVolc, and SIVlho lineages. Nevertheless, in the gag gene, this observation must be viewed with caution due to the high degree of divergence characterized by the long branches within this clade, as well as a low posterior probability value (91%). In the Pol1 tree, the relationships between SIVwrc, SIVolc, SIVlho, and SIVcol is supported by high posterior probability values and suggests a clear ancestral link between these different SIV lineages in this part of the genome. Genetic distance analysis strengthens this observation with 68 to 71% amino acid identities between SIVwrc, SIVlho, SIVolc, and SIVcol lineages (Table 2).

In the Env protein, SIVwrc and SIVolc lineages form a highly supported cluster with the SIVlho lineage, as well as with SIVmnd-2 and SIVdrl, which are known to cluster with SIVmnd-1 and SIVlho/sun in Env. Interestingly, in Env, SIVwrc and SIVolc appear to be more closely related to SIVmnd-1/mnd-2/drl than to SIVlho/sun. Amino acid identities (56 to 61% versus 51 to 54%) further illustrate this relationship (Table 2).

In addition to the group of SIVs (SIVsyk, SIVdeb, SIVden, SIVgsn, SIVmus, and SIVmon) that infects members of the Cercopithecus genus, we observed that SIVs derived from western red and olive colobus, mandrills, and L'Hoest and suntailed monkeys, form a second group of viruses which cluster consistently together in phylogenetic trees. We also observed fluctuating relationships for other lineages across the different tree topologies. For example, the SIVcpz lineage that is described as a recombinant strain between both SIVrcm and SIVgsn ancestor lineages forms a distinct monophyletic group in Gag and Pol2 tree, thus suggesting a more complex natural history and evolution than previously described (3). Overall, these results highlight the complexity of disentangling the phylogenic relationships within the primate lentiviruses as more genomic data become available.

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In this study we describe the full-length genome sequences for SIVs derived from two Colobinae species, each belonging to a different genus, SIVwrc from western red colobus (Piliocolobus badius badius) and SIVolc from olive colobus (Procolobus verus) inhabiting the Taï forest in the south-eastern part of Ivory Coast. We confirmed that geographically isolated subspecies of the western red colobus, in The Gambia and Ivory Coast are infected with closely related species-specific SIVs, and that Western red colobus are thus the natural hosts of SIVwrc (31). We also showed that SIVolc is a distinct species-specific lineage, but more closely related to the SIVwrc lineage than to any other SIV across almost the entire length of its genome. Overall, SIVs derived from western red and olive colobus, mandrills, L'Hoest and suntailed monkeys, form a group of viruses that cluster consistently together in phylogenetic trees.

The common evolutionary history of SIVwrcPbb and SIVwrcPbt is not surprising because animals of the two Piliocolobus subspecies may have shared gene flow until recently, and their ranges, which are poorly documented, could still overlap (53). The genetic diversity between SIVolc and SIVwrc is significantly higher than among SIVs from the different subspecies of western red colobus and is thus most likely the result of an ancient cross-species transmission or an infection by a common ancestor. It will thus be important to characterize additional SIVolc strains from wild olive colobus in other geographic areas in order to determine to what extent this species is infected with SIV and also to identify whether SIVolc is the result of an ancestral cross-species transmission between red colobus and olive colobus from the Taï forest in Ivory Coast, the only region where their habitats overlap. It will also be interesting to study more in detail western red and olive colobus in the Taï forest, where they live in polyspecific primate associations, to examine to what extent cross-species transmissions still occur.

Overall, SIVwrc and SIVolc are most closely related to the SIVlho/sun lineage across the whole genome. Interestingly, SIVcol, which represents a divergent SIV lineage, is also closely related to SIVwrc, SIVolc, and the SIVlho lineage in the 5' part of Pol and to a lower extent in Gag. The relationships between these different SIV lineages are somewhat surprising because of the geographical separation of their hosts. The characterization of these new SIVwrc and SIVolc lineages raises thus more questions than answers regarding the evolution of SIVs. The three species carrying SIVs from the SIVlho lineage (SIV mnd-1 from M. sphinx, SIVlho from C. lhoesti, and SIVsun from C. solatus) are all confined to Central Africa. The ranges of the different Piliocolobus and Colobus species and subspecies cover discontinuously the west-African forest blocks extending into central-eastern Africa (Fig. 1 and 5). Although the actual range of certain Piliocolobus and Colobus species overlaps that of C. lhoesti superspecies to the east of the Democratic Republic of Congo and to the southwest of Cameroon, their habitats do not overlap at all with the West African species (Fig. 5). In order to better understand the evolution of SIVs in the colobines, it will be important to characterize additional SIVs in the remaining species of Colobus and Piliocolobus genera across Africa. Particular attention should be paid to Piliocolobus and Colobus species whose ranges overlap today with those of the Cercopithecus species harboring SIVlho and SIVsun. This will help to determine whether the virus emerged before or after speciation or geographic separation events among colobids and will provide further insight into the importance of biogeographic barriers and cross-species transmission in SIV evolution (Fig. 5). Especially, it will be important to study whether black and white colobus (Colobus polykomos) species in the Taï forest are infected and characterize their SIV.

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FIG. 5. Ranges occupied by the different species and subspecies of Piliocolobus (in blue), including those overlapping with the C. lhoesti superspecies (C. lhoesti, C. solatus, C. preussi, and C. insularis) and the colobus monkeys (in red).

It is now well established that the evolutionary history of primate lentiviruses has been driven by host-virus coevolution, cross-species transmission, and recombination events over an extended period of time. Indeed, the description of new SIVwrc and SIVolc strains renders the evolutionary history of primate lentiviruses even more difficult to disentangle but shows that apparently two major groups of SIV lineages can be observed: one previously described that comprises the SIVs from the majority of the Cercopithecus species (6) and one observed in the present study comprising SIVs from western red and olive colobus, SIVs from L'Hoest and suntailed monkeys, and SIVmnd-1 from mandrills. This suggests that there are two SIV lineages in Cercopithecus: one for arboreal and one for semiterrestrial species (C. lhoesti and C. solatus). However, studies on the evolution of the primate hosts show that C. lhoesti and C. solatus do not cluster with the other species of the Cercopithecus genus but form a clade with semiterrestrial species (Erytrocebus and Chlorocebus spp.), suggesting a taxonomic revision for C. lhoesti and C. solatus (54, 62). The majority of colobids are arboreal species, and therefore the distinction between an arboreal and a terrestrial SIV lineage cannot be generalized beyond the actual Cercopithecus genus. However, geographic isolation and ecological factors such as vegetation type and distribution can shape or elicit new or different behaviors and exceptional cases of colobids with semiterrestrial behavior and living in polyspecific associations with semiterrestrial species have been documented, e.g., P. badius temminckii in The Gambia (13, 31). These different polyspecific associations could play a role in cross-species transmission and recombination of divergent SIVs and explain the clustering of SIVwrc, SIVolc, SIVlho, SIVsun, and SIVmnd-1.

In addition to the relationship of SIVs from colobids from West Africa and L'Hoest and suntailed monkeys from Central Africa, the relationship between SIVlho/sun and SIVmnd-1 remains also an enigma. Mandrills and monkeys from the L'Hoest superspecies are phylogenetically distant species within the Cercopithecinae and inhabit geographically separate regions of Central Africa. Only the range of SIVsun-infected suntailed monkeys overlaps with that of mandrills in Gabon, south of the Ogoue River (Fig. 5). However, SIVsun is more distantly related to SIVmnd than to SIVlho and might not have been the proximal source of SIVmnd. Different hypotheses tried to explain this close relationship, and one of these involved a yet-unidentified SIV in another primate species (4). Given the relationship between SIVwrc and SIVlho/sun, another red colobus species could be involved. In Cameroon, the habitats from Piliocolobus penantii preussi overlap with that of mandrills and could be a possible candidate for the missing links. However, this area is also inhabited by the Cercopithecus preussi from the lhoesti superspecies, and the characterization of SIVs in this species will also provide more insights on the origin of SIVs in mandrills (Fig. 5). Overall, knowledge of primate behavior and past and recent geographic distribution of the different primate species could add important complementary information to understanding the evolutionary history of SIVs in nonhuman primates.

Importantly, humans and chimpanzees (Pan troglodytes verus) commonly hunt western red colobus for food (47), and humans also hunt chimpanzees. Numerous P. troglodytes versus samples have been analyzed, but no evidence for SIV infections has been reported yet, despite the high SIVwrc prevalence in their preys. The majority of these chimpanzee samples were obtained from wild caught animals, which are usually captured when infants (45, 51), in which the prevalences are generally lower. However, the absence of SIV infection could also be due to unadapted serologic and/or molecular tools, the majority of P. troglodytes versus samples have been screened with HIV-1-specific Western blots, which are maybe not able to efficiently detect cross-reactive antibodies of SIVwrc. The increasing acquisition of SIV sequences will allow us to develop new serologic and molecular tools in order to document with higher accuracy new SIV infections in wild Old word primates and to screen human populations to define whether cross-species transmissions with other SIVs occurred. The human population around the Taï forest still frequently hunts primates, and western red colobus represents an important part of the bushmeat monkeys (27, 42). Moreover, we previously documented high SIV prevalences in P. badius badius from the Taï forest (32). The ancestors of the two epidemic strains from HIV-2, group A and B, are derived from SIV that still circulate in wild mangabey populations from the Taï forest (44), illustrating the need for surveillance of primate pathogens and their cross-species transmissions in this part of Africa and elsewhere.

 
This study was supported by grants from the Agence Nationale de Recherche sur le Sida (ANRS-12125) and from the National Institutes of Health (R01AI50529).

We thank Ronald Noë and Christophe Boesch for logistical assistance in the field and Chantal Koffi-Akoue for assistance with sample handling.

 
* Corresponding author. Mailing address: UMR 145, Institut de Recherche pour le Développement, 911, Avenue Agropolis, 34394 Montpellier, France. Phone: (33) 0467416297. Fax: (33) 0467416146. E-mail: martine.peeters{at}mpl.ird.fr

Published ahead of print on 15 October 2008.

Present address: Environmental Microbial Genomics Group, UMR CNRS 5005/EC-INSA-UCBL, Ecole Centrale de Lyon, Ecully, France.

Present address: Institut de Génétique Moléculaire de Montpellier, CNRS UMR5535, Université Montpellier 1 et 2, Montpellier, France.

Top ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1
1. Aghokeng, A. F., E. Bailes, S. Loul, V. Courgnaud, E. Mpoudi-Ngolle, P. M. Sharp, E. Delaporte, and M. Peeters. 2007. Full-length sequence analysis of SIVmus in wild populations of mustached monkeys (Cercopithecus cephus) from Cameroon provides evidence for two co-circulating SIVmus lineages. Virology 360:407-418.[CrossRef][Medline]
2
2. Allan, J. S., M. Short, M. E. Taylor, S. Su, V. M. Hirsch, P. R. Johnson, G. M. Shaw, and B. H. Hahn. 1991. Species-specific diversity among simian immunodeficiency viruses from African green monkeys. J. Virol. 65:2816-2828.[Abstract/Free Full Text]
3
3. Bailes, E., F. Gao, F. Bibollet-Ruche, V. Courgnaud, M. Peeters, P. A. Marx, B. H. Hahn, and P. M. Sharp. 2003. Hybrid origin of SIV in chimpanzees. Science 300:1713.[Free Full Text]
4
4. Beer, B. E., E. Bailes, R. Goeken, G. Dapolito, C. Coulibaly, S. G. Norley, R. Kurth, J. P. Gautier, A. Gautier-Hion, D. Vallet, P. M. Sharp, and V. M. Hirsch. 1999. Simian immunodeficiency virus (SIV) from sun-tailed monkeys (Cercopithecus solatus): evidence for host-dependent evolution of SIV within the C. lhoesti superspecies. J. Virol. 73:7734-7744.[Abstract/Free Full Text]
5
5. Beer, B. E., B. T. Foley, C. L. Kuiken, Z. Tooze, R. M. Goeken, C. R. Brown, J. Hu, M. St Claire, B. T. Korber, and V. M. Hirsch. 2001. Characterization of novel simian immunodeficiency viruses from red-capped mangabeys from Nigeria (SIVrcmNG409 and -NG411). J. Virol. 75:12014-12027.[Abstract/Free Full Text]
6
6. Bibollet-Ruche, F., E. Bailes, F. Gao, X. Pourrut, K. L. Barlow, J. P. Clewley, J. M. Mwenda, D. K. Langat, G. K. Chege, H. M. McClure, E. Mpoudi-Ngole, E. Delaporte, M. Peeters, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 2004. New simian immunodeficiency virus infecting De Brazza's monkeys (Cercopithecus neglectus): evidence for a cercopithecus monkey virus clade. J. Virol. 78:7748-7762.[Abstract/Free Full Text]
7
7. Bibollet-Ruche, F., C. Brengues, A. Galat-Luong, G. Galat, X. Pourrut, N. Vidal, F. Veas, J. P. Durand, and G. Cuny. 1997. Genetic diversity of simian immunodeficiency viruses from West African green monkeys: evidence of multiple genotypes within populations from the same geographical locale. J. Virol. 71:307-313.[Abstract]
8
8. Clewley, J. P., J. C. Lewis, D. W. Brown, and E. L. Gadsby. 1998. A novel simian immunodeficiency virus (SIVdrl) pol sequence from the drill monkey, Mandrillus leucophaeus. J. Virol. 72:10305-10309.[Abstract/Free Full Text]
9
9. Courgnaud, V., P. Formenty, C. Akoua-Koffi, R. Noe, C. Boesch, E. Delaporte, and M. Peeters. 2003. Partial molecular characterization of two simian immunodeficiency viruses (SIV) from African colobids: SIVwrc from Western red colobus (Piliocolobus badius) and SIVolc from olive colobus (Procolobus verus). J. Virol. 77:744-748.[CrossRef][Medline]
10
10. Courgnaud, V., X. Pourrut, F. Bibollet-Ruche, E. Mpoudi-Ngole, A. Bourgeois, E. Delaporte, and M. Peeters. 2001. Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family. J. Virol. 75:857-866.[Abstract/Free Full Text]
11
11. Daniel, M. D., Y. Li, Y. M. Naidu, P. J. Durda, D. K. Schmidt, C. D. Troup, D. P. Silva, J. J. MacKey, H. W. Kestler III, P. K. Sehgal, et al. 1988. Simian immunodeficiency virus from African green monkeys. J. Virol. 62:4123-4128.[Abstract/Free Full Text]
12
12. Dazza, M. C., M. Ekwalanga, M. Nende, K. B. Shamamba, P. Bitshi, D. Paraskevis, and S. Saragosti. 2005. Characterization of a novel vpu-harboring simian immunodeficiency virus from a Dent's Mona monkey (Cercopithecus mona denti). J. Virol. 79:8560-8571.[Abstract/Free Full Text]
13
13. DeMenocal, P. 2004. African climate change and faunal evolution during the pliocene-Pleistocene. Earth Planetary Sci. Lett. 220:3-24.[CrossRef]
14
14. Dimmic, M. W., J. S. Rest, D. P. Mindell, and R. A. Goldstein. 2002. rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J. Mol. Evol. 55:65-73.[CrossRef][Medline]
15
15. Ekwalanga, M. R. K., M. Dazza, M. Nende, K. Shamamba, and S. Saragosti. 2002. Molecular characterization of a primate lentivirus from Cercopithecus wolfi, abstr. TuPeA4417. Abstr. XIV International AIDS Conference, Barcelona, Spain.
16
16. Emau, P., H. M. McClure, M. Isahakia, J. G. Else, and P. N. Fultz. 1991. Isolation from African Sykes' monkeys (Cercopithecus mitis) of a lentivirus related to human and simian immunodeficiency viruses. J. Virol. 65:2135-2140.[Abstract/Free Full Text]
17
17. Freed, E. O. 2002. Viral late domains. J. Virol. 76:4679-4687.[Free Full Text]
18
18. Gao, F., E. Bailes, D. L. Robertson, Y. Chen, C. M. Rodenburg, S. F. Michael, L. B. Cummins, L. O. Arthur, M. Peeters, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 1999. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436-441.
19
19. Georges-Courbot, M. C., C. Y. Lu, M. Makuwa, P. Telfer, R. Onanga, G. Dubreuil, Z. Chen, S. M. Smith, A. Georges, F. Gao, B. H. Hahn, and P. A. Marx. 1998. Natural infection of a household pet red-capped mangabey (Cercocebus torquatus torquatus) with a new simian immunodeficiency virus. J. Virol. 72:600-608.[Abstract/Free Full Text]
20
20. Groves, C. 2001. Primate taxonomy. Smithsonian series in comparative evolutionary biology. Smithsonian Institution Press, Washington, DC.
21
21. Hahn, B. H., G. M. Shaw, K. M. De Cock, and P. M. Sharp. 2000. AIDS as a zoonosis: scientific and public health implications. Science 287:607-614.[Abstract/Free Full Text]
22
22. Hirsch, V. M., B. J. Campbell, E. Bailes, R. Goeken, C. Brown, W. R. Elkins, M. Axthelm, M. Murphey-Corb, and P. M. Sharp. 1999. Characterization of a novel simian immunodeficiency virus (SIV) from L'Hoest monkeys (Cercopithecus lhoesti): implications for the origins of SIVmnd and other primate lentiviruses. J. Virol. 73:1036-1045.[Abstract/Free Full Text]
23
23. Hirsch, V. M., C. McGann, G. Dapolito, S. Goldstein, A. Ogen-Odoi, B. Biryawaho, T. Lakwo, and P. R. Johnson. 1993. Identification of a new subgroup of SIVagm in tantalus monkeys. Virology 197:426-430.[CrossRef][Medline]
24
24. Hirsh, V. M., R. A. Olmsted, M. Murphey-Corb, R. H. Purcell, and P. R. Johnson. 1989. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339:389-392.
25
25. Jin, M. J., H. Hui, D. L. Robertson, M. C. Muller, F. Barre-Sinoussi, V. M. Hirsch, J. S. Allan, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 1994. Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO J. 13:2935-2947.[Medline]
26
26. Keele, B. F., F. Van Heuverswyn, Y. Li, E. Bailes, J. Takehisa, M. L. Santiago, F. Bibollet-Ruche, Y. Chen, L. V. Wain, F. Liegeois, S. Loul, E. M. Ngole, Y. Bienvenue, E. Delaporte, J. F. Brookfield, P. M. Sharp, G. M. Shaw, M. Peeters, and B. H. Hahn. 2006. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523-526.[Abstract/Free Full Text]
27
27. Kormos, R., M. I. Bakarr, L. Bonnéhin, and R. Hanson-Alp. 2004. La chasse pour la viande de brousse et les chimpanzés en Afrique de l'Ouest. IUCN-Primates Specialist Group, Gland, Switzerland.
28
28. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5:150-163.[Abstract/Free Full Text]
29
29. Liegeois, F., V. Courgnaud, W. M. Switzer, H. W. Murphy, S. Loul, A. Aghokeng, X. Pourrut, E. Mpoudi-Ngole, E. Delaporte, and M. Peeters. 2006. Molecular characterization of a novel simian immunodeficiency virus lineage (SIVtal) from northern talapoins (Miopithecus ogouensis). Virology 349:55-65.[CrossRef][Medline]
30
30. Ling, B., C. Apetrei, I. Pandrea, R. S. Veazey, A. A. Lackner, B. Gormus, and P. A. Marx. 2004. Classic AIDS in a sooty mangabey after an 18-year natural infection. J. Virol. 78:8902-8908.[Abstract/Free Full Text]
31
31. Locatelli, S., B. Lafay, F. Liegeois, N. Ting, E. Delaporte, and M. Peeters. 2008. Full molecular characterization of a simian immunodeficiency virus, SIVwrcpbt from Temminck's red colobus (Piliocolobus badius temminckii) from Abuko Nature Reserve, The Gambia. Virology 376:90-100.[CrossRef][Medline]
32
32. Locatelli, S., F. Liegeois, B. Lafay, A. D. Roeder, M. W. Bruford, P. Formenty, R. Noe, E. Delaporte, and M. Peeters. 2008. Prevalence and genetic diversity of simian immunodeficiency virus infection in wild-living red colobus monkeys (Piliocolobus badius badius) from the Taï forest, Cote d'Ivoire SIVwrc in wild-living western red colobus monkeys. Infect. Genet. Evol. 8:1-14.[CrossRef][Medline]
33
33. Lowenstine, L. J., N. C. Pedersen, J. Higgins, K. C. Pallis, A. Uyeda, P. Marx, N. W. Lerche, R. J. Munn, and M. B. Gardner. 1986. Seroepidemiologic survey of captive Old-World primates for antibodies to human and simian retroviruses, and isolation of a lentivirus from sooty mangabeys (Cercocebus atys). Int. J. Cancer 38:563-574.[Medline]
34
34. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 2001. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7:1313-1319.[CrossRef][Medline]
35
35. McGraw, W. S., K. Zuberbühler, and R. Noë. 2005. Monkeys of the Taï Forest. Cambridge Studies in Biological and Evolutionary Anthropology no. 51. Cambridge University Press, Cambridge, United Kingdom.
36
36. Pandrea, I., R. Onanga, P. Rouquet, O. Bourry, P. Ngari, E. J. Wickings, P. Roques, and C. Apetrei. 2001. Chronic SIV infection ultimately causes immunodeficiency in African non-human primates. AIDS 15:2461- 2462.[CrossRef][Medline]
37
37. Peeters, M., V. Courgnaud, B. Abela, P. Auzel, X. Pourrut, F. Bibollet-Ruche, S. Loul, F. Liegeois, C. Butel, D. Koulagna, E. Mpoudi-Ngole, G. M. Shaw, B. H. Hahn, and E. Delaporte. 2002. Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg. Infect. Dis. 8:451-457.[Medline]
38
38. Peeters, M., K. Fransen, E. Delaporte, M. Van den Haesevelde, G. M. Gershy-Damet, L. Kestens, G. van der Groen, and P. Piot. 1992. Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. AIDS 6:447-451.[Medline]
39
39. Peeters, M., C. Honore, T. Huet, L. Bedjabaga, S. Ossari, P. Bussi, R. W. Cooper, and E. Delaporte. 1989. Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS 3:625-630.[Medline]
40
40. Puffer, B. A., L. J. Parent, J. W. Wills, and R. C. Montelaro. 1997. Equine infectious anemia virus utilizes a YXXL motif within the late assembly domain of the Gag p9 protein. J. Virol. 71:6541-6546.[Abstract]
41
41. Ray, S. 1999. SImPlot version 2.5 software documentation. SCRoftware, Baltimore, MD.
42
42. Refisch, J., and I. Kone. 2005. Market hunting in the Taï region, Côte d'Ivoire, and implication for monkey populations. Int. J. Primatol. 26:621-629.[CrossRef]
43
43. Salemi, M., T. De Oliveira, V. Courgnaud, V. Moulton, B. Holland, S. Cassol, W. M. Switzer, and A. M. Vandamme. 2003. Mosaic genomes of the six major primate lentivirus lineages revealed by phylogenetic analyses. J. Virol. 77:7202-7213.[Abstract/Free Full Text]
44
44. Santiago, M. L., F. Range, B. F. Keele, Y. Li, E. Bailes, F. Bibollet-Ruche, C. Fruteau, R. Noe, M. Peeters, J. F. Brookfield, G. M. Shaw, P. M. Sharp, and B. H. Hahn. 2005. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Taï Forest, Cote d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J. Virol. 79:12515-12527.[Abstract/Free Full Text]
45
45. Santiago, M. L., C. M. Rodenburg, S. Kamenya, F. Bibollet-Ruche, F. Gao, E. Bailes, S. Meleth, S. J. Soong, J. M. Kilby, Z. Moldoveanu, B. Fahey, M. N. Muller, A. Ayouba, E. Nerrienet, H. M. McClure, J. L. Heeney, A. E. Pusey, D. A. Collins, C. Boesch, R. W. Wrangham, J. Goodall, P. M. Sharp, G. M. Shaw, and B. H. Hahn. 2002. SIVcpz in wild chimpanzees. Science 295:465.[Free Full Text]
46
46. Souquiere, S., F. Bibollet-Ruche, D. L. Robertson, M. Makuwa, C. Apetrei, R. Onanga, C. Kornfeld, J. C. Plantier, F. Gao, K. Abernethy, L. J. White, W. Karesh, P. Telfer, E. J. Wickings, P. Mauclere, P. A. Marx, F. Barre-Sinoussi, B. H. Hahn, M. C. Muller-Trutwin, and F. Simon. 2001. Wild Mandrillus sphinx are carriers of two types of lentivirus. J. Virol. 75:7086-7096.[Abstract/Free Full Text]
47
47. Stanford, C. 1998. To catch a colobus, p. 84-87. In Primate anthology: essays on primate behavior, ecology, and conservation from natural history. Prentice Hall, Upper Saddle River, NJ.
48
48. Strack, B., A. Calistri, S. Craig, E. Popova, and H. G. Gottlinger. 2003. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114:689-699.[CrossRef][Medline]
49
49. Takehisa, J., Y. Harada, N. Ndembi, I. Mboudjeka, Y. Taniguchi, C. Ngansop, S. Kuate, L. Zekeng, K. Ibuki, T. Shimada, B. Bikandou, Y. Yamaguchi-Kabata, T. Miura, M. Ikeda, H. Ichimura, L. Kaptue, and M. Hayami. 2001. Natural infection of wild-born mandrills (Mandrillus sphinx) with two different types of simian immunodeficiency virus. AIDS Res. Hum. Retrovir. 17:1143-1154.[CrossRef][Medline]
50
50. Takemura, T., M. Ekwalanga, B. Bikandou, E. Ido, Y. Yamaguchi-Kabata, S. Ohkura, H. Harada, J. Takehisa, H. Ichimura, H. J. Parra, M. Nende, E. Mubwo, M. Sepole, M. Hayami, and T. Miura. 2005. A novel simian immunodeficiency virus from black mangabey (Lophocebus aterrimus) in the Democratic Republic of Congo. J. Gen. Virol. 86:1967-1971.[Abstract/Free Full Text]
51
51. Teleki, G. 1989. Population status of wild chimpanzees and threats to survival, p. 313-353. In P. G. Heltne and L. A. Marquardt (ed.), Understanding chimpanzees. Harvard University Press, Cambridge, MA.
52
52. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.[Abstract/Free Full Text]
53
53. Ting, N. 2008. Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys. J. Hum. Evol. 55:312-325.[CrossRef][Medline]
54
54. Tosi, A. J., N. J. Melnick, and T. R. Disotell. 2003. Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). J. Human Evol. 46:223-237.[CrossRef]
55
55. Traina-Dorge, V., J. Blanchard, L. Martin, and M. Murphey-Corb. 1992. Immunodeficiency and lymphoproliferative disease in an African green monkey dually infected with SIV and STLV-I. AIDS Res. Hum. Retrovir. 8:97-100.[Medline]
56
56. Tsujimoto, H., R. W. Cooper, T. Kodama, M. Fukasawa, T. Miura, Y. Ohta, K. Ishikawa, M. Nakai, E. Frost, G. E. Roelants, et al. 1988. Isolation and characterization of simian immunodeficiency virus from mandrills in Africa and its relationship to other human and simian immunodeficiency viruses. J. Virol. 62:4044-4050.[Abstract/Free Full Text]
57
57. Tsujimoto, H., A. Hasegawa, N. Maki, M. Fukasawa, T. Miura, S. Speidel, R. W. Cooper, E. N. Moriyama, T. Gojobori, and M. Hayami. 1989. Sequence of a novel simian immunodeficiency virus from a wild-caught African mandrill. Nature 341:539-541.
58
58. Van Heuverswyn, F., Y. Li, C. Neel, E. Bailes, B. F. Keele, W. Liu, S. Loul, C. Butel, F. Liegeois, Y. Bienvenue, E. M. Ngolle, P. M. Sharp, G. M. Shaw, E. Delaporte, B. H. Hahn, and M. Peeters. 2006. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444:164.
59
59. Verschoor, E. J., Z. Fagrouch, I. Bontjer, H. Niphuis, and J. L. Heeney. 2004. A novel simian immunodeficiency virus isolated from a Schmidt's guenon (Cercopithecus ascanius schmidti). J. Gen. Virol. 85:21-24.[Abstract/Free Full Text]
60
60. von Schwedler, U. K., M. Stuchell, B. Muller, D. M. Ward, H. Y. Chung, E. Morita, H. E. Wang, T. Davis, G. P. He, D. M. Cimbora, A. Scott, H. G. Krausslich, J. Kaplan, S. G. Morham, and W. I. Sundquist. 2003. The protein network of HIV budding. Cell 114:701-713.[CrossRef][Medline]
61
61. Wertheim, J. O., and M. Worobey. 2007. A challenge to the ancient origin of SIVagm based on African green monkey mitochondrial genomes. PLoS Pathog. 3:e95.[CrossRef][Medline]
62
62. Xing, J., H. Wang, Y. Zhang, D. A. Ray, A. J. Tosi, T. R. Disotell, and M. A. Batzer. 2007. A mobile element-based evolutionary history of guenons (tribe Cercopithecini). BMC Biol. 5:5.[CrossRef][Medline]
63
63. Yang, Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J. Mol. Evol. 39:306-314.[CrossRef][Medline]
64
64. Yang, Z., and B. Rannala. 1997. Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method. Mol. Biol. Evol. 14:717-724.[Abstract]

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Journal of Virology, January 2009, p. 428-439, Vol. 83, No. 1
0022-538X/09/$08.00+0     doi:10.1128/JVI.01725-08
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