Given that humans are nouveaux riches regarding our collection of infections [5], can we infer further examples of infections that could have come from other hominid species or from more distantly related primates? The infections for which we have the most accurate evolutionary record are the endogenous retroviruses that have invaded host DNA. Some 8% of the human genome represents 'fossil' integrated proviruses. The human lineage accumulated several thousand retroviral genomes after the split between New World and Old World primates, but only a handful since we diverged from chimpanzees.

Parasites that have tightly cospeciated with their hosts are, of course, in grave danger of extinction when that host becomes an endangered species. But the 'smart' parasite would gain a whole new lease of evolutionary opportunity if it engaged in occasional 'infidelity', analogous to mutation in DNA replication. A DNA lineage that does not mutate would have an extraordinarily slow rate of evolution, whereas a super-mutator without repair would provide little opportunity for natural selection before the genotype changed further. Thus, a low mutation rate within broad fidelity of DNA replication allows for both inheritance and evolution. Likewise, total cospeciation dooms the parasite to the fate of the host, whereas the ability to move horizontally to closely related hosts would provide flexibility. Parasite jumping between related hosts might occur more frequently than realized because it might easily be overlooked.

By this reckoning, the New World clade of head lice formerly faithful to the H. erectus lineage [2] adopted modern humans in the nick of time. HIV-1 might well be another successful case of jumping off a sinking ship, because its former host is not likely to survive for many generations longer in the wild. Now that HIV-1 has adopted a new host species, it is enjoying a most successful adaptive radiation and has already colonized around 60 million humans (25 million of whom have died from AIDS). Such crossover events, however, are relatively rare, and only one of the three ape-to-human transfers of HIV-1 has taken off to cause the AIDS pandemic [11]. It pays the host to place barriers known as restriction factors in the path of potential pathogens. If a species barrier is not recognized by the new invader or is successfully circumvented, the infection can be more virulent in the new host.

Regarding the intestinal parasites and ectoparasites that specialize in human infestation, Ashford [6] pointed out that we not only house two kinds of closely related lice (he meant Pediculus head and body lice), but also two species of Cimex bedbugs, two of Demodex mites and two of Taenia tapeworms. He therefore asked if we were once two separate populations that rejoined after a long separation, but Ashford did not have DNA sequences and molecular clock estimates available to him. Can we now view this phenomenon in the same way as the lice, as one of the pair of parasites cospeciating with H. sapiens and the other jumping from non-ancestral archaic humans to the modern human lineage? It would be intriguing to conduct similar molecular phylogenies of Ashford's other pairs.

Ashford [6] finished by stating: "Over to the microbiologists: What do the bacteria, viruses and fungi tell us?" There are ample examples both of cospeciation and horizontal transmission. The malaria parasite Plasmodium falciparum exemplifies a complex cospeciation between the parasite, its human host and its mosquito vector. Anopheles gambiae has also coevolved to be a specialist feeder on humans; by contrast, the other human malaria parasite, P. vivax, has an origin in South East Asian monkeys and is transmitted by the more promiscuous Culex species. Might vivax malaria have first adapted to H. erectus as an intermediate between monkeys and humans?

As a virologist, I have felt stimulated [23] to take up Ashford's challenge to consider pairs of related human viruses. HIV-1 and HIV-2 are very recent 20th century arrivals, from chimpanzees and sooty mangabey monkeys, respectively. With human T-cell lymphotropic viruses types 1 and 2 (HTLV-1 and HTLV-2), there have been multiple introductions of HTLV-1 from African and Asian monkeys and apes [25]. The provenance of HTLV-2 is puzzling, as its reservoir is in indigenous American populations and in African pygmies, which are as far apart in H. sapiens as one can find. Humans have five distinct polyoma viruses and multiple genital papilloma virus types. The different clades of hepatitis C virus (HCV) have deep roots but there are no known animal relatives to provide an anchor or time calibration. It would be fascinating to learn whether archaic humans harbored HCV variants, but as HCV has an RNA genome there is not much hope of gaining direct evidence by sequence amplification from ancient specimens.

All members of the herpesvirus family are thought to have strictly cospeciated with their hosts, though I have my doubts. The closest relatives to human herpes simplex virus (an α herpesvirus), cytomegalovirus (β) and Epstein-Barr virus (γ), seem to be those in the chimpanzee. Several simian species have a pair of distinct rhadinoviruses, whereas so far humans are only known to harbor one, Kaposi's sarcoma herpesvirus. On the other hand, humans have two herpes simplex viruses (HSVs), types 1 and 2. Phylogenetic analysis [26] indicates that HSV-1 and HSV-2 are further apart from each other than HSV-1 is from its chimp ortholog [27]. So where did HSV-2 come from? From its estimated age of divergence from the chimp-human HSV-1 lineage, I would place a bet on horizontal transmission from gorillas or possibly from orang-utans [23].

Is it a coincidence that three human parasites acquired horizontally from great apes, namely pubic lice, HIV-1 and speculatively HSV-2, are sexually transmitted? Now, before one conjures up a King Kong scenario, it should be noted that predators can pick up parasites from their prey. The close contact involved in human ancestors butchering gorillas could have enabled Pthirus to jump hosts, rather as bushmeat slaughter practices probably led SIVcpz and other retroviruses to invade humans from chimpanzees in modern times [11, 25].