Virolution. Frank Ryan
or three countries away, like Ghana, that are distinguishable from the HIV-2 infecting people in Senegal, which is 80km away – even though the viruses in people and monkeys in each country are not distinguishable from each other.’
I sat back to reflect on what Essex was telling me. The simian immunodeficiency virus and the human immunodeficiency virus, HIV-2, are actually one and the same virus. In his words: ‘It’s just that you call it one thing if it’s in people and another thing if it’s in mangabey monkeys.’ But there was a further, crucial, implication of what he had discovered. We believe that HIV-1, the main virus of AIDS, was transferred to people from a specific group of chimpanzees. We also know that, in chimpanzees, HIV-1 grows freely and reproduces in their internal organs and tissues, but it causes no evidence of disease. And like HIV-1 in chimpanzees, SIV produces no evidence of disease in mangabey monkeys, even though the virus also multiples freely in the monkeys’ tissues. Yet it seems altogether likely that, on first contact between the viruses and these animal hosts, the viral behaviour is likely to have been very aggressive. If we need any confirmation, we only need recall what happened when the SIV-carrying African mangabeys were housed in the same facility as the Asian macaques at the facility near Harvard. No more is it surprising that when chimpanzees, carrying an SIV virus closely related to what we now recognise as HIV-1, came into contact with people, the forerunner of HIV-1 hopped species to cause the aggressively fatal AIDS in humans.
I posed some relevant questions:
‘Let us say that a particular virus has been infecting an animal for a very long time and the animal and virus have reached the stage where they are coexisting without the virus causing serious disease in the animal. Now say another species of animal – a similar species – comes into contact with the host. It seems likely that the virus will cross species in a very vicious manner – it may prove to be highly lethal. Is it possible that what we are seeing here is an evolutionary mechanism? I also ask myself this: What if this is a symbiotic pattern of evolution, a symbiotic relationship between virus and host? In these circumstances, what might the host animal be getting out of it? And what occurs to me is that one of the things it could be getting out of it is the advantage that if a rival, for food or whatever, comes into its ecological niche, the virus jumps species and wipes out the rival.’
‘Yes, I think that’s a very logical hypothesis. You know the system that most shaped my own thoughts on that and made me write some of the things I did, such as the Scientific American article in which I compound the monkey virus behaviour in the different species with Frank Fenner’s discussion of the myxomatosis epidemic in Australia. And the bottom line of that is that when Europeans brought captive rabbits into Australia for the first time, the rabbits escaped into the wild. And because there were no foxes or natural enemies to control the rabbit populations, they multiplied in numbers and started destroying the crops. So the people there decided they needed to kill off the rabbits. They brought in a myxomatosis virus that those rabbits had not seen before. The myxomatosis virus they brought in killed right away – because it spread very well – some 99.8% of the rabbits. But then two things happened. Number one – within four years, the resistant minority grew so you had a different population of disease-resistant rabbits. Now, even if you brought in a virulent strain it didn’t kill them. And number two – the myxomatosis virus that remained [as a persistent infection in the rabbits] was less virulent, so I think there is crystal-clear evidence that both the host and the virus attenuated themselves for optimal survival in that situation. Now, were you to bring in new rabbits, the new rabbits would be disadvantaged. The surviving rabbits still live with the virus but they are now resistant, so that they can then be totally healthy and function normally while retaining a myxomatosis virus that is still virulent enough to prove a threat to any rival rabbits coming in.’
I pressed him a little further: ‘I’m aware also that certain herpes viruses appear to be particularly venomous when they cross species in monkeys. Is it your opinion that we are seeing the same thing?’
‘Oh, absolutely! I think that some of the most dramatic examples in primates are viruses like Herpesvirus simiri and anteles. They have co-evolved in one species of monkey, like spider or squirrel monkey, and when you put them into contact with any other species of monkey they are highly, highly lethal, but in the resident co-evolving species they do nothing.’
‘Would you agree that, here again, we’re looking at an example of an evolutionary role?’
‘My guess is you could even find evidence that the monkeys that are most susceptible occupy the same ecological niche and are eating the same food, as opposed to some of the ones, even if they cover the same territory, that eat a different food and fit a different living niche, and that are not quite as susceptible [to the virus].’
When two or more partners enter into a mutualistic symbiosis, each partner will contribute an innate ability, or trait, that the other partner lacks. It is obvious what a host contributes to a virus-host partnership, since it offers the virus shelter and the use of the host’s own genetic machinery to make more copies of itself. Without the host, the virus would not survive. But although it might appear less obvious, there is in fact a key ability that the virus possesses – in evolutionary terms, a “trait” – that the host does not. This is the innate potential for lethal aggression. In the example of Elysia chlorotica, we witnessed how the retroviruses that are long-established partners within its nucleus and tissues, may end the slug’s life cycle with what appears to be a ferocious demonstration of aggression. In fact, following my researches into viral behaviour, in Virus X, I first put forward the evolutionary concept of “aggressive symbiosis” as an important mechanism – I have never claimed it to be an exclusive one – in a number of situations in nature, and in particular in the interaction between plague viruses and their hosts. But coining the mechanism was merely the first step in the hypothesis I was attempting to formulate. I now had to figure out how such a mechanism might work, in evolutionary terms, as part of the evolving partnerships of viruses and their hosts in nature.
I began by making a couple of reasonable assumptions. Up to this time, virtually all evolutionary research within the discipline of virology had been Darwinian in concept. I was familiar with its conclusions, which were central to medical virology, and, by and large, I agreed with them. I also took the view that Darwinism and symbiogenesis were not mutually exclusive. There was overwhelming evidence that both mechanisms operated in nature. This suggested that each virus-host relationship needed to be examined in its own right: but it also needed to be examined through the binocular vision of both evolutionary mechanisms, and not merely through one. Sometimes the dominant mechanism would fit the Darwinian paradigm, such as the operation of selection at selfish individual, or selfish gene, level. Sometimes the dominant mechanism would more closely fit the symbiotic paradigm, with selection operating to an important degree at the level of the partnership of virus and host. Indeed, I saw no reason why, in certain situations, both paradigms would not apply, with a dynamic that might start with dominance at selfish level, but might evolve to end up with a dominant effect at partnership level. This would fit with the original thinking of de Bary. Moreover, it would also fit with the mathematical derivations of two Oxford-based Professors, Anderson and May, who, in the early 1990s, had spent a lot of time examining virus-host dynamics, including co-evolution – a Darwinian concept that came very close to the symbiotic concept of partnership.
Over the ensuing years, I continued to work on the dynamic of emerging plague viruses, and I discovered that aggressive symbiosis worked through a series of very specific steps. It began when the virus invaded a new, or virgin, host. The interaction could result in a variety of different behaviours, depending on whether the virus came from a closely related species, and was thus pre-evolved in its infectious strategies, or whether it came from a more distantly related species, when its infectious strategies would not be so efficiently pre-evolved. The Sin Nombre hantavirus came from a rodent and, though it killed a high percentage of the people it infected, it could not efficiently transmit between people. Several recently notorious viruses Marburg, Ebola, Lassa fever and the South American haemorrhagic fever viruses, such as Machupo and Junin, did exactly the same. Lassa, Machupo and Junin all came from rodents and were not sufficiently transmissible between people. While the hosts of Marburg and Ebola were still uncertain, their failure to transmit efficiently between