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Diversity and Evolution of Primate Lentiviruses

Brigitte E. Beer1, Elizabeth Bailes2, Paul M. Sharp2, and Vanessa M. Hirsch1*

  1. Laboratory of Molecular Microbiology, National Institute of Allergy and Infectious Diseases, National Institute of Health, Rockville, Maryland 20852,
  2. Institute of Genetics, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, United Kingdom

    *corresponding author

INTRODUCTION

The human immunodeficiency viruses (HIV-1 and -2) together with the simian immunodeficiency viruses (SIV) comprise the primate lentivirus family. Since the isolation of the first SIV in 1985 [15], our knowledge of the diversity of these primate lentiviruses has continuously developed by the isolation and characterization of new SIV strains from additional species of African simians. It is now clear that the SIVs are a large group of viruses that can be found naturally in feral and domesticated African primates, such as guenons, mangabeys, mandrills, and chimpanzees; to indicate the species from which each SIV was isolated they are given a short suffix, such as SIVagm for the virus derived from African green monkeys. Most of these African primates are natural hosts for these viruses, but some infections are the result of recent cross-species transmissions. In those species that are natural hosts, the proportion of animals that are seropositive in the wild can be quite high [5, 33, 55, 60], and infected primates do not seem to develop any clinical symptoms [22, 51, 66]. The reasons for this lack of pathogenicity are still not well understood. However the lack of pathogenicity does not seem to be based on inherent properties of the virus, since for example Asian macaques inoculated with SIV from sooty mangabeys or African green monkeys can develop AIDS-like symptoms similar to those of humans after HIV infection [35, 59]. Because SIV is the most closely related lentivirus to HIV, SIV infection of monkeys has become the best animal model for studying the pathogenesis of, and efficacy of vaccines against, HIV infection in humans. In addition, the evaluation of new SIV strains is important to better understand the origins of HIV-1 and -2 and to assess the potential for additional lentiviruses to infect the human population.

PHYLOGENY OF PRIMATE LENTIVIRUSES

SIV infection has been detected in more than 20 different species of African primates, but examples of complete sequences of only 13 of these are available to date (Table 1). As shown in Fig. 1, these fully characterized SIVs can be classified into five distinct lineages based upon phylogenetic analyses of their sequences [37, 68, 70]. These five lineages are represented by (i) SIVcpz from chimpanzees (Pan troglodytes) [24, 40, 42, 64, 83], (ii) SIVsm from sooty mangabeys (Cercocebus atys) [11, 39, 56, 65, 66], (iii) SIVagm from four species of African green monkeys (recently re-named as the Chlorocebus genus) [2, 4, 16, 20, 21, 38, 43, 45, 58, 73], (iv) SIVsyk from Sykes' monkeys (Cercopithecus albogularis) [19, 36], and (v) SIVlhoest from L'Hoest monkeys (Cercopithecus lhoesti). These five lineages are approximately equidistant, differing from each other at about 40 of amino acid residues in the Pol protein.

Four of these major lineages (the exception being SIVsyk) are represented by multiple strains including isolates from two or more host species; the SIVs within one lineage cluster together with high bootstrap values (Fig. 1). From the evolutionary tree, it is evident that the distinction between HIV and SIV reflects only whether a virus is found in humans or some other species of primate and is not an accurate taxonomic classification since HIV-1 and HIV-2 are not each others' closest relatives. In fact, HIV-1 is closely related to lentiviruses from chimpanzees, while HIV-2 clusters with viruses infecting sooty mangabeys (Fig. 1). Thus, from these and other observations, it can be concluded that the human AIDS viruses have arisen quite recently through cross-species transmissions from these two other primates in Africa.




Table 1  Full length genome sequences of primate lentiviruses

Source Strain/isolate Accession# Author Reference
1. SIVcpz lineage (Pan troglodytes subspecies) P. t. troglodytes SIVcpzGab1 X52154 Huet T (1990) Nature 345, 356 SIVcpzUS AF103818 Gao F (1999) Nature 397, 436 SIVcpzCam3 AF115393 Corbet S (2000) J Virol 74, 529 P. t. schweinfurthii SIVcpzAnt U42720 Vanden Haesevelde M Virology 221, 346 (1996)
2. SIVsm lineage (Cercocebus atys and Macaca species) C. atys SIVsmH4 X14307 Hirsch V (1989) Nature 339, 389 SIVsmE543 U72748 Hirsch V (1997) J Virol 71, 1608 SIVsm9 M80194 Courgnaud V (1992) J Virol 66, 414 SIVsmPBjA.4.41 M31325 Dewhurst S (1990) Nature 345, 636 SIVsmPBj6.6 L09212 Novembre F (1993) J Virol 67, 2466 SIVsmPGm AF077017 Novembre F (1998) J Virol 72, 8841 M. mulatta SIVmm239 M33262 Regier D (1990) ARHR 6, 1221 SIVmm251 M19499 Franchini G (1987) Nature 328, 539 SIVmm32H D01065 Rud E (1994) J Gen Virol 75, 529 SIVmm1A11 M76764 Luciw P (1992) ARHR 8, 395 SIVmm142 M16403 Chakrabarti L (1987) Nature 328, 543 M. nemestrina SIVmne8 M32741 Benveniste R (1990) unpublished SIVmne027 U79412 Kimata J (1998) J Virol 72, 245 M. arctoides SIVstm M83293 Novembre F (1992) Virology 186, 783
3. SIVagm lineage (Chlorocebus species) C. pygerythrus SIVagmVerTyo X07805 Fukasawa M (1988) Nature 333, 457 SIVagmVer155 M29975 Johnson P (1990) J Virol 64, 1086 SIVagmVer3 M30931 Baier M (1990) Virology 176, 216 SIVagmVer9063 L40990 Hirsch V (1995) J Virol 69, 955 C. aethiops SIVagmGri677 M66437 Fomsgaard A (1991) Virology 182, 397 C. tantalus SIVagmTan1 U58991 Soares M (1997) Virology 228, 394 C. sabaeus SIVagmSab1C U04005 Jin M (1994) EMBO J 13, 2935
4. SIVsyk lineage (Cercopithecus albogularis) C. albogularis SIVsyk173 L06042 Hirsch V (1993) J Virol 67, 1517
5. SIVlhoest lineage (Cercopithecus species and Mandrillus sphinx) M. sphinx SIVmndGB1 M27470 Tsujimoto H (1989) Nature 341, 539 C. lhoesti SIVlhoest7 AF075269 Hirsch V (1999) J Virol 73, 1036 SIVlhoest447 AF188114 Beer B (2000) J Virol, in press SIVlhoest485 AF188115 Beer B (2000) J Virol, in press SIVlhoest524 AF188116 Beer B (2000) J Virol, in press C. solatus SIVsun1 AF131870 Beer B (1999) J Virol 73, 7734

aAll isolates originate from sooty mangabeys and have been passaged intentionally or unintentionally to macaques. The first column indicates the species, in which the isolate was first identified. For passage history see Human Retroviruses and AIDS 1998: A Compilation and Analysis of Nucleic Acid and Amino Acid Sequences. Korber B, Kuiken CL, Foley B, Hahn B, McCutchan F, Mellors JW, and Sodroski J, Eds. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM. p. III-94. Brackets indicate that virus isolates/clones share a common passage history.



Figure 1: Evolutionary relationships among primate lentiviruses. The tree was derived by maximum likelihood analysis of Pol protein sequences. Horizontal branch lengths are drawn to scale. A similar tree was derived by neighbor-joining analysis; asterisks denote clades (to the right) supported in at least 80 of bootstrap replicates. GENOMIC ORGANIZATION

The basic common, and presumably ancestral, structure for primate lentiviruses is LTR-gag- pol-vif-vpr-tat-rev-env-nef-LTR. These viral genes overlap in a number of regions (Fig. 2). The tat and rev genes consist of two exons (exon 2 lies within the env open reading frame) whereas the other six genes have only one exon. This basic structure applies to the members of the SIVagm, SIVsyk, and SIVlhoest lineages [3, 6, 20, 21, 34, 35, 38, 43, 45, 73]. The viruses belonging to the SIVcpz and SIVsm lineages each have one additional gene. SIVsm-related viruses, including HIV-2 and SIVmac, have a vpx gene upstream of the vpr gene [47]. The deduced Vpx protein shares sequence similarity with Vpr, and therefore could have been arisen through a tandem gene duplication [78], although phylogenetic analyses suggest that vpx is more likely to have been acquired by nonhomologous recombination between different SIVs [69]. The vpu gene occurs upstream of, and overlapping, env in SIVcpz from chimpanzees and HIV-1 [24, 40, 76, 83]. A vpu gene has not been found in the genomes of other SIVs, although the extent of divergence of the Vpu protein even among SIVcpz [83] is so great as to indicate that vpu homologues elsewhere would be difficult to recognize on the basis of sequence similarity. The origin of vpu has not been elucidated.

Figure 2: Genomic organization of the primate lentivirus lineages. PRIMATE EVOLUTION

To understand the evolution of the SIVs, and in particular to ascertain whether SIVs have been evolving in parallel with their hosts for a long period of time, or whether there have been other instances of cross-species transmission (between non-human primates), it is necessary to consider the phylogenetic relationships among those primate hosts (Fig. 3). Within the primate evolutionary tree, apes such as humans and chimpanzees are highly divergent from the Old World monkeys, which include all the other species from which primate lentiviruses have been isolated. Furthermore, within the Old World monkeys, Sykes' and L'Hoest monkeys (both classified in the genus Cercopithecus) and African green monkeys (the genus Chlorocebus) are much more closely related to each other than to mangabeys (Cercocebus spp.). Thus, the approximate equidistance among the five major lineages of SIV does not match the relationships among their hosts. In addition, Asian species of primates such as macaques, as well as some African species such as baboons of the genus Papio, do not appear to be naturally infected with their own species-specific SIV. These observations imply that the last common ancestor of the catarrhines (Old World monkeys and apes) around 25 million years ago was not infected by SIV, but that one of these primate species became infected by an ancestral lentivirus from a non-primate source at a later time point. In the last two decades, lentiviruses have been isolated from various other orders of mammals [29, 61, 67, 74, 75], but none of those characterized is specifically closely related to the primate viruses. Once SIV was established in the primate population, simian-to-simian cross-species transmissions occurred, on the deeper branches within the SIV tree. THE SIVcpz/HIV-1 LINEAGE

The only examples of SIV that are closely related to HIV-1 come from chimpanzees (Fig. 1). Since the vast majority of AIDS cases worldwide are due to infection with HIV-1, sequences of vastly

Figure 3: Evolutionary relationships among catarrhine primates (Old World monkeys and apes). The tree is schematic only, having been synthesized from a variety of sources including analyses of genetic and morphological markers: it summarizes what appears to be the consensus of views on relationships among species, but branch lengths are at best approximate. Major sources: references [17, 27, 31, 81].

more isolates of HIV-1 have been determined than of any other primate lentivirus. In contrast, rather few examples of SIVcpz have been characterized as yet. Two wild-caught chimpanzees from Gabon were first reported to be seropositive for HIV-1 antibodies more than 10 years ago [64]. A full-length genome sequence was characterized for one (SIVcpzGab1) [40], but only a 280 bp pol fragment for the other (SIVcpzGab2) [42]. A third isolate, SIVcpzAnt, was obtained from a chimpanzee wild-caught in the Democratic Republic of Congo (formerly Zaire) [63, 83]. Only within the last year have four more isolates been reported, one from a captive animal in the United States that had been imported from Africa as a juvenile [24], and three from chimpanzees in Cameroon [14]. In light of recent genetic evidence to support the division of chimpanzees into four distinct subspecies [23, 57], all of these animals have, in some cases retrospectively, been characterized at the mitochondrial DNA level. As expected, the two animals from Gabon, and two of those from Cameroon, were found to belong to the central African subspecies, Pan troglodytes troglodytes, while the chimpanzee from the Democratic Republic of Congo was a member of the East African subspecies P. t. schweinfurthii [24]. The animal from the US was found to be another P. t. troglodytes [24], while the third chimpanzee from Cameroon belonged to the Nigerian subspecies, P. t. vellerosus [14].

These subspecies assignments are of particular interest in interpreting the phylogenetic relationships among the SIVcpz isolates, and the relationship between SIVcpz and HIV-1 (Fig. 4). First, since it was first characterized and still to this date, SIVcpzAnt has been recognized as being highly divergent from all other SIVcpz. Since SIVcpzAnt is the only isolate from P. t. schweinfurthii, this

Figure 4: Evolutionary relationships among members of the SIVcpz/HIV-1 lineage. The tree was derived by maximum likelihood analysis of Env protein sequences. Horizontal branch lengths are drawn to scale. Adapted from [30]. could be interpreted as the result of an ancient split between the viruses infecting different subspecies of chimpanzee [24], similar to the divergence among clades of SIV infecting different species of African green monkeys (see below). In contrast, the isolate from P. t. vellerosus (SIVcpzCam4) is extremely closely related to one of the isolates from P. t. troglodytes (SIVcpzCam3), obtained from an animal at the same location. This level of identity is indicative of epidemiological linkage. This suggests that the P. t. vellerosus animal most likely became infected in captivity, and leaves open the question of whether P. t. vellerosus, as well as the fourth subspecies, the West African chimpanzee P. t. verus, are naturally infected with SIVcpz in the wild.

In the past, the apparently low prevalence of SIV infection in chimpanzees, as well as other factors including the high degree of divergence between SIVcpzAnt and other isolates, had cast doubt on whether chimpanzees are the natural reservoir for this group of lentiviruses. The possibility existed that both humans and chimpanzees had acquired these viruses from some other, unidentified, species of African primate. However, the recent increase in the number of characterized SIVcpz isolates, together with the information about the subspecies from which they were isolated, and considerations about the geographical origins of SIVcpz and HIV-1, have all combined to indicate that chimpanzees have indeed been the proximal source of HIV-1 [14, 24]. On the basis of phylogenetic relationships, HIV-1 isolates have been classified into three distinct clades, groups M, N and O ([71]; see also the article by Robertson et al., in this volume). In comparisons involving SIVcpz, the three groups of HIV-1 are not each others' closest relatives, and so they must each have arisen from a separate cross-species transmission event [24, 71]. All three groups of HIV-1 are more closely related to the SIVcpz isolates from P. t. troglodytes than to that from P. t. schweinfurthii (Fig. 4), indicating that the former subspecies, and not the latter, has been the source of HIV-1 [14, 24]. This is consistent with the geographical origins of the HIV-1 groups. The P. t. troglodytes subspecies inhabits Cameroon, Gabon and surrounding countries in west equatorial Africa: group N has only so far been reported in that region, group O is largely restricted to the same area, and while group M has achieved global distribution, the greatest diversity of group M subtypes is found in west equatorial Africa.

THE SIVsm/SIVmac/HIV-2 LINEAGE

The second human AIDS virus, HIV-2, has been found to be closely related to SIVs isolated from macaques and sooty mangabeys. First evidence for a virus of this lineage appeared in the early 1980s when an unusual clustering of lymphomas and immunodeficiency-associated disorders (similar to AIDS in humans) was noted in a colony of captive rhesus macaques (Macaca mulatta) at the New England Regional Primate Research Center [41, 53, 54]. These observations led to the isolation of a T-cell tropic retrovirus, initially called STLV-III (now re-named SIVmac or SIVmm), which was shown to be antigenically related to HTLV-III (now called HIV-1) [46]. Subsequently, SIV was isolated from other macaque species. At the Washington Regional Primate Research Center, SIVmne was recovered from stored lymph node tissue of a pig-tailed macaque (Macaca nemestrina) that died of lymphoma in 1982 [7]; and at the California Regional Primate Research Center, SIVstm was isolated from frozen tissues of a stump-tailed macaque (Macaca arctoides) that had died of lymphoma and AIDS-like symptoms in the mid-1970s [49]. In 1986, a second human AIDS virus, named HIV-2, was isolated from patients with acquired immune deficiency syndrome (AIDS) originating from West Africa. Molecular analyses revealed that HIV-2 was genetically related to SIV from macaques [12].

However, very few macaques in captivity, and none in the wild in Asia, were found to be infected with SIV [84]. The natural origin of this form of SIV remained unresolved for several years. Then, molecular characterization of a virus from captive sooty mangabeys (Cercocebus atys), designated SIVsm, revealed that it was closely related to HIV-2 and SIVs from macaques [39]. In subsequent years, SIVsm strains were isolated from free-ranging and pet sooty mangabeys in their natural habitat in West Africa (Guinea-Bissau to Ivory Coast) [10, 11, 56]. Thus, it seems likely that SIVmm, SIVmne and SIVstm resulted from unintentional transmissions of SIV from sooty mangabeys to macaques in captivity.

The close relationship between SIVsm and HIV-2 from humans suggested that feral SIV-infected sooty mangabeys in West Africa might be the natural source for HIV-2 infection in humans [39]. In the last decade, several lines of supporting evidence for this epidemiological link have been provided [9--11, 25, 26, 56]. HIV-2 is a diverse group of viruses consisting of six different clades, termed subtypes A--F [9, 25]. Several of the HIV-2 subtypes have only been found in West Africa, in countries within the range of free-living sooty mangabeys. Furthermore, strains of SIVsm from different sooty mangabeys are known to be highly diverse, differing by up to 19 in gag nucleotide sequences [10, 11, 56]. Importantly, the various HIV-2 subtypes are not more closely related to one another than to SIVsm strains [11]. Instead, the HIV-2 and SIVsm lineages are phylogenetically interspersed (Fig. 5). Additionally, geographic clustering between SIVsm and HIV-2 strains in Sierra Leone and Liberia has been demonstrated. This indicates that the different clades of HIV-2 cannot all be due to a single mangabey-to-human transmission but must be the result of multiple independent cross-species transmissions of SIVsm into the human population. The observation of cross-species transmission of SIVsm is not surprising as sooty mangabeys are often kept as pets and used for food in West Africa [56]. Moreover, SIVsm has been shown to be transmissible to humans after accidental exposure to monkey blood [48].

THE SIVagm LINEAGE

Among feral primates that are known to be infected with SIV the African green monkeys are the most numerous, most geographically dispersed, and the most commonly infected [1, 2, 33, 38, 58, 60]. African green monkeys are dispersed over most of sub-Saharan Africa and have been classified as a separate genus (Chlorocebus) which is comprised of four species [52]: grivet (Chlorocebus aethiops), vervet (Chlorocebus pygerythrus), tantalus (Chlorocebus tantalus), and sabaeus (Chlorocebus sabaeus). These four species are distinguishable on the basis of phenotypic and genotypic markers and have different geographic ranges. Grivets live in Ethiopia and the Sudan, vervets can be found from East to South Africa, tantalus monkeys are prevalent in central Africa and sabaeus monkeys are restricted to West Africa.

Initially, SIVs from AGMs were described as one virus group with a novel and extremely high degree of genetic diversity [4, 45]. Later it was found that the four species of African green monkeys each

Figure 5: Evolutionary relationships among members of the SIVsm/SIVmac/HIV-2 lineage. The (unrooted) tree was derived by neighbor-joining analysis of partial gag nucleotide sequences. Branch lengths are drawn to scale, and percentage bootstrap values greater than 50 are shown. Adapted from reference [9]; kindly provided by Dr. P. A. Marx. carry their own species-specific SIV indicating that the distinct forms of SIVagm may have evolved in parallel to their hosts. According to their host species, the SIVagm isolates have been named SIVagmVer, SIVagmGri, SIVagmSab, and SIVagmTan [2, 4, 16, 20, 21, 38, 43, 45, 58, 73]. SIVagmVer is the most extensively characterized group and many molecular clones have been generated including SIVagmVer3, SIVagmVer9063, SIVagmVer155, and SIVagmVerTyo (Table 1) [3, 21, 35, 45]. There is as much as 20 divergence in the Pol protein among SIVagmVer isolates [35] and 30 divergence in the Gag protein between SIVagmGri-1 and SIVagmVer155 [45, 73]. SIVagm from sabaeus monkeys (SIVagmSab) is unusual because it was found to have a mosaic genome structure. Parts of the genome (3 end of gag and 5 end of pol) cluster with the SIVsm/HIV-2 lineage whereas the rest of the genome groups with the SIVagm lineage [43]. This indicates that recombination between divergent SIVs occurred during the evolution of SIVagmSab, and also implies that cross-species transmission among simians provided the opportunity for this recombination to occur. The two viral lineages involved, SIVagmSab and SIVsm, both infect monkeys from West Africa. The hybrid virus has been successful in that it is the only form of SIV that has been found among sabaeus monkeys.

Sporadic instances of SIVagm-like viruses have been reported from species other than African green monkeys, apparently reflecting recent simian-to-simian cross-species transmission in the wild. For example, two (out of 279 tested) wild-living yellow baboons (Papio hamadryas cynocephalus) from an area of Tanzania also inhabited by vervets were reported to harbor antibodies reactive with a SIVagm-like antigen [50]. It was later demonstrated that a virus isolated from one of these animals clustered within the vervet viruses in gag and env phylogenies [44]. Similarly, a chacma baboon (Papio ursinus) from South Africa was found to be infected with a virus strain of SIVagm most closely related to SIV from South African vervets. [82]. In another study, a wild-living patas monkey (Erythrocebus patas) in Senegal was found to be infected with a strain of SIVagm most closely related to those from sympatric sabaeus monkeys [8]. Additionally, a captive white-crowned mangabey (Cercocebus lunulatus) has been found to be infected with virus closely related to SIVagm from a vervet [77]. This transmission probably occurred in captivity because white-crowned mangabeys are indigenous to West Africa, where sabaeus monkeys are the local species of African green monkeys.

THE SIVsyk LINEAGE

Similar to African green monkeys, Sykes' monkeys (Cercopithecus albogularis) exhibit a high rate of SIV seroprevalence [19]. So far, only one full-length molecular clone of SIVsyk has been described and characterized [36], and no closely related viruses have been found in any other species. In contrast to the SIV strains from the other four lineages, SIVsyk has a very restricted host cell tropism in vitro, because it preferentially replicates in CD4+ enriched peripheral blood mononuclear cells (PBMC) from Sykes' monkeys and not in human, mangabey, or macaque PBMC [19]. However, macaques inoculated in vivo with SIVsyk became persistently infected but remained clinically healthy [36].

THE SIVlhoest LINEAGE

This lineage includes viruses isolated from three different species, the L'Hoest monkey (Cercopithecus lhoesti), the sun-tailed monkey (Cercopithecus solatus), and the mandrill (Mandrillus sphinx). The mandrill virus, SIVmndGB1, from an animal in Gabon, was first described more than 10 years ago [79, 80], and for many years was the only known representative of the ``SIVmnd'' lineage. However, recently characterized isolates of SIVlhoest and SIVsun have been found to lie within the same major lineage as SIVmnd [5, 6, 34]. The ranges of mandrills and sun-tailed monkeys overlap in west equatorial Africa, whereas L'Hoest monkeys inhabit an area approximately 1600 km to the east. Nevertheless, SIVlhoest and SIVsun are more closely related to each other than to SIVmnd (Fig. 1). The close relationship of SIVlhoest and SIVsun parallels the close relationship between their two host species (Fig. 3), which have been placed in the same superspecies [32]; mandrills are only distantly related to these guenons. L'Hoest monkeys appear to be infected with SIV at quite high frequencies in the wild [5]. Taken together, these observations suggest that this lineage of SIV has infected monkeys of this C. lhoesti superspecies for quite some time, and that the split between SIVlhoest and SIVsun may have occurred when their hosts last shared a common ancestor before they became geographically isolated. This appears to be an additional example of host-dependent evolution paralleling that in SIVs from African green monkeys. Since the frequency of this SIV isolate in wild-living mandrills is unclear, and because a highly divergent form of SIV has recently been reported from other mandrills [72], we have recently suggested that this viral clade should be designated the SIVlhoest lineage rather than the SIVmnd lineage [6].

The presence of quite closely related viruses in quite distantly related hosts (guenons and mandrills) indicates that cross-species transmission must have occurred at some point in the past. Because of their close relationship to one another, neither SIVlhoest nor SIVsun can have been the direct ancestor of SIVmnd. It is possible that SIV was transmitted from mandrills to a common ancestor of L'Hoest and sun-tailed monkeys, although it perhaps seems more likely that the Cercopithecus monkeys were the species infected first. It will be interesting to determine whether Preuss's monkeys (Cercopithecus preussi), which are closely related to L'Hoest and sun-tailed monkeys (Fig. 3, [18, 32]), and whose range also overlaps that of mandrills, are naturally infected with SIV, and how such a virus might be related to SIVlhoest and SIVsun (and SIVmnd).

UNCLASSIFIED PRIMATE LENTIVIRUSES

There is at least serological evidence for SIV infection in a number of other species of African monkeys, and there are even more species that have yet to be tested in any systematic way. Viruses have been isolated from some species, and partial sequence data are available for several. These strains do not seem to be very closely related to any of the previously characterized SIV, although the precise phylogenetic positions of these novel isolates must probably await analysis of full-length sequences.

One of these new variants, SIVrcm, was isolated from the red-capped mangabey (Cercocebus torquatus) [28]. Red-capped mangabeys are very closely related to sooty mangabeys (Fig. 3) and in some classifications have been placed within the same species. However, SIVrcm does not appear to be closely related to SIVsm [28]. In a phylogenetic analysis based on partial (318 amino acids) Gag sequences, SIVrcm was approximately equidistant from the SIVsm and SIVagm lineages. However, in an analysis of partial (155 amino acids) Pol sequences, SIVrcm was more closely related to the SIVcpz/HIV-1 clade than to any of the other major lineages. The discordance between these results suggests that there has been recombination between SIV lineages in the past, similar to that inferred to have occurred during the evolution of SIVagmSab.

Another recently characterized SIV was obtained from the drill (Mandrillus leucophaeus) [13]. Drills are closely related to mandrills (Fig. 3), but SIVdrl was not found to be closely related to SIVmndGB1. Phylogenetic analysis of partial (787 bp) pol sequences suggested that SIVdrl was more closely related to SIVrcm than to any other SIV, although the SIVdrl and SIVrcm nucleotide sequences differ by nearly 30 [13]. It is not known whether SIVdrl and SIVrcm would also cluster together in a gag phylogeny.

Serological studies have indicated that talapoin monkeys (Miopithecus talapoin) are infected by lentiviruses. A small fragment (550 bp) of pol sequence has been obtained from one such virus (SIVtal) and found to be most closely, albeit quite distantly, related to SIVsyk [62]. SIVtal and SIVsyk exhibit only 56 amino acid sequence identity in the region studied, and so SIVtal may represent a sixth distinct lineage of the primate lentiviruses. However, as with SIVrcm and SIVdrl, definitive conclusions about the phylogenetic position of SIVtal should be based on analyses of more extensive sequence data.

Antibodies to SIV proteins have been found in sera from De Brazza's monkeys (Cercopithecus neglectus), moustached monkeys (C. cephus), Diana monkeys (C. diana), greater white-nosed monkeys (C. nictitans), Campbell's monkeys (C. campbelli), Allen's swamp monkeys (Allenopithecus nigroviridis), and Colobus monkeys (Colobus guereza) [6, 55, 60]. Clearly, it will be of great interest to isolate and characterize viruses from these species. Such analysis will be necessary to gain a greater insight into the origins and evolution of the primate lentiviruses, to understand exactly how widespread they are among African primates, and to elucidate just how often they have successfully jumped between host species.

CONCLUSIONS

The primate lentiviruses are a diverse group, that naturally infect African species of simians. SIVs from 13 different species have been fully characterized, and within evolutionary trees, they cluster into five approximately equidistant major lineages. However, serological evidence exists for SIVs in a large number of additional species, some of which have been partially characterized, with results that hint at even greater complexity in the primate lentivirus evolutionary tree. Within some major SIV lineages there are viral radiations that seem to reflect speciation events among their hosts, implying that these SIVs may have been evolving in a host-dependent manner for a long period of time. However, there have clearly been many instances of simian-to-simian cross-species transmissions, some of which have led to widespread infection of the new host. Simian-to-human transmissions, from chimpanzees and sooty mangabeys, have led to HIV-1 and HIV-2, respectively, and thus lie at the origin of the AIDS pandemic.

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