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The AIDS Pandemic Is New, but Is HIV Not New?

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The AIDS Pandemic Is New, but Is HIV Not New? Cladistics 13, 267–273 (1997) WWW http://www.apnet.com Forum The AIDS Pandemic is New, but is HIV Not New? Mark E. Siddall Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48109, U.S.A. Accepted 17 June 1997 The determinations made by Mindell, Shultz and Ewald methods, Mindell et al. (1995) concluded that HIV was regarding the ancestral host for immunodeficiency retro- not a “new virus” and, contrary to conventional belief, viruses, and their conclusion that monkeys acquired that monkeys acquired their retroviruses from their infections as a result of a host-switch from humans, humans. Knowledge about the history of the human do not withstand rigorous scrutiny. Their hypothesis immunodeficiency viruses (HIV1 and HIV2) can have requires the complete uniformativeness of third position a bearing on expected results for disease intervention transitions and of gapped regions in the alignment. strategies and for the expectations that vaccination When all of the data are permitted to corroborate or refute relationships, optimizing hosts on the viral phyl- regimes will be successful. Different assessment of the ogeny renders either equivocal statements or an relative age of the origin of primate immunodeficiency unequivocal simian ancestry. However, merely optimiz- viruses (PIV) will lead to different conclusions regard- ing hosts as characters on the viral phylogeny is illogical. ing mutation rates, and retroviruses with faster Not only does this treat hosts as dependent on the mutation rates are not good candidates for vaccine viruses (instead of the reverse) but it ignores 15 years of development (Atlan et al., 1994). Also there are methodological developments specifically designed to sociological, anthropological and transmission consid- answer questions regarding cospeciation or host-switch- erations regarding the relative order of appearance of ing. © 1997 The Willi Hennig Society the immunodeficiency viruses. So far as is known, HIV transmission requires direct contact with virus-laden fluids (e.g. blood, blood products, and semen) for Acquired immunodeficiency syndrome (AIDS) was transmission to occur. The retroviral envelope, which unknown prior to the early 1980s. When HIV was is necessary for infection of cells, renders the virions determined to be the cause of the disease, it was natu- susceptible to degradation. It is this Achilles heel, the rally assumed to be a “new virus” (new to infecting envelope, which renders fomite transmission unlikely humans). It is, however, possible that HIV is an “old (because of desiccation) and vector-borne transmission virus” which had been present in human populations routes nearly impossible (because of rapid digestion of and only recently became virulent. Using phylogenetic lipids in the gastrointestinal tracts of blood-feeding dipterans or leeches). These elements of the host–para- Correspondence to: M. E. Siddall, E-mail: [email protected], site system are consistent with humans having recently Fax: (313) 663 4080. acquired the virus from green monkeys. In light of this, 0748-3007/97/030267+07/$25.00/0/cl970044 Copyright © 1997 by The Willi Hennig Society All rights of reproduction in any form reserved 267 268 Siddall the findings by Mindell et al. (1995: 83) are unusual in that “within the HIV2/SIVsm/SIVmac/SIVagm clade, human is also shown as the ancestral host species”, and FIV SIVsyk SIVmnd HIV1jrc HIV1lai HIV1rf HIV1eli HIV1ndk HIV1mal SIVcpz HIV1mvp HIV1ant70 SIVagm3 SIVagtyo SIVagm155 SIVagm677 HIV2uc1 HIV2d205 HIV2ben HIV2d194 HIV2rod HIV2nihz HIV2st SIVstm SIVsmm9 SIVsmmh4 SIVsmm239 SIVmne that “the more parsimonious scenario indicates virus transmission from humans (HIV2s) to sooty mangabeys and macaques” (emphasis added). Humans do not regularly bite monkeys, or share needles with them, nor is there evidence of humans being hunted and eaten by arboreal green monkeys, macaques or mang- abeys. This leaves us having to postulate alternative primate behavioural patterns regarding HIV transmis- sion from humans to monkeys, or be concerned that (A) Ancestral host is ambiguous mosquitoes could transmit the virus after all. The conclusions drawn by Mindell et al. (1995) can Falis Cercopithecus be shown to be dependent on their perspective on the Homo Mandrillus data and on the manner in which hosts were dealt Pan Macaca with. Fig. 1 reproduces the most parsimonious tree Cercocebus Equivocal found by Mindell et al. (1995) for PIV relationships. In it, HIV1 and HIV2 are hypothesized as having separate origins which is consistent with the present viral nomenclatural designations. The most parsimonious reconstruction of ancestral host type, when each host FIV SIVsyk SIVmnd HIV1jrc HIV1lai HIV1rf HIV1eli HIV1ndk HIV1mal SIVcpz HIV1mvp HIV1ant70 SIVagm3 SIVagtyo SIVagm155 SIVagm677 HIV2uc1 HIV2d205 HIV2ben HIV2d194 HIV2rod HIV2nihz HIV2st SIVstm SIVsmm9 SIVsmmh4 SIVsmm239 SIVmne species is taken as a discrete characteristic of the virus (sensu Mindell et al., 1995) is that humans are the ances- tral source of the virus. For each host species to be considered a characteristic of the virus requires strict host specificity. However, even the findings of Mindell et al. (1995) suggest a remarkable lack of host specific- ity. That is, with at least six host-switches (transformations on their tree), the viruses cannot be (B) Ancestral host is said to be very specific. Although the data were pre- ambiguous or sented as individual isolates from individual species, is simian there is no evidence that the three isolates from Cat Human macaques (SIVstm, SIVmne, and SIVmm239) are nec- Simian essarily restricted to the host species from which they Equivocal were obtained. Nor has this been suggested for the five viruses infecting Cercopithecus species (SIVsyk, FIG. 1. The most parsimonious reconstructions of host characters SIVagm677, SIVagm155, SIVagm3, and SIVagtyo). when defined as genera (A) and when defined more generally (B) Supposing, for the moment, that the viruses at least are have different implications for determining whether or not humans restricted by genus of host (Fig. 1A), the original ances- are suggested as the ancestral host. In the latter perspective, the ori- tral host type becomes ambiguous. The available data, gins of the viruses are completely equivocal (tree redrawn from however, refute even genus-level specificity. Various Mindell et al., 1995). viruses from Cercopithecus species are unconstrained by species boundaries. The 1967 outbreak of Marburg agent of human herpesviridae infection (Martin et al., virus demonstrated that the Ebola-like filoviridae can 1995). The primate immunodeficiency virus of green kill humans infected from green monkey body fluids monkeys is no exception. In natural populations, green (Halstead, 1981). Similarly, a cytomegalovirus from monkey SIVs readily infect other cercopithecids green monkeys has been revealed as the etiological (Bibolett-Ruche et al., 1996) and even baboons (Jin et Copyright © 1997 by The Willi Hennig Society All rights of reproduction in any form reserved Forum: Reassessing HIV Origins 269 al., 1994). In this light the question should have been a more general human versus monkey dichotomy. How- FIV ever, this renders all of the ancestral host optimizations SIVmnd equivocal (Fig. 1B). 21 HIV1jrc 31 Mindell et al. (1995: 83) suggested that their topology HIV1lai 53 HIV1rf was “preferable because of its incorporation of more HIV1eli character evidence”. However, they did not actually 198 42 HIV1ndk include all of the character evidence. Their hypothesis 38 HIV1mal was predicated on the complete uninformativeness of 142 SIVcpz transitions in the third positions of codons and also of 218 HIV1mvp all gapped regions. That is, third positions in codons HIV1ant70 received zero weight and gapped regions were 39 SIVagm3 excluded. This practice, though defended by Mindell 117 SIVagtyo 24 94 et al. (1995) in terms of concerns regarding swamping SIVagm155 3 of phylogenetic signal by noise, is a contentious issue SIVagm677 in systematics (Bryant, 1989; Hillis, 1991; Collins et al., SIVsyk 1994) and it has yet to be shown that noise will always 172 HIV2uc1 24 HIV2d205 swamp a signal (Rieppel, 1989). Even if third-position 9 41 HIV2ben transitions are expected to be problematic at ancient HIV2d194 nodes (Mindell et al., 1995: table 1), those transitions 106 HIV2st 18 may yet be expected to be informative regarding recent 200 5 HIV2nihz divergences. Insofar as the working hypothesis was HIV2rod Host switch that human infection has been the result of a recent SIVstm to humans 34 divergence, data relevant to these recent phenomena 109 SIVsmm9 should not have been excluded, or the difference that 43 SIVsmmh4 this makes in the resulting hypothesis should at least Cat 159 SIVmm239 have been acknowledged. I have reanalysed the PIV Human SIVmne data set1 in light of these concerns. Use of Farris et al.’s Simian (1994) incongruence measure indicated that none of Equivocal the excluded portions of data were significantly heter- FIG. 2. The most parsimonious tree obtained using all of the data ogenous with the included data. That is, for each of the unweighted, all of the data with successive approximations, and all four genes, treating gapped regions as a partition ren- of the data with third-position transitions downweighted according dered a tail probability of incongruence between 0.70 to their estimated frequency. Bremer (1988) support indices are and 0.18 and for third positions in codons versus first given at each node. Reconstruction
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