different from that. In these cases there is an integration of genetic machinery, even though the interacting genomes are still distinct. The symbionts are in different cells, and they could be parted asunder. But I see a continuum between that phenomenon and the kinds of symbiosis where the two organisms occupy the same cell, such as we see in plants with their chloroplasts. It’s not so difficult to extrapolate from that to the evolution of invertebrates, where you have algae living in the epidermal cells. But what we find in the chloroplast has taken the concept further. The primordial chloroplast has itself exchanged considerable numbers of genes with the nucleus. Meanwhile, some genes that were undoubtedly nuclear have found their way into the chloroplasts. So these have not been pure genomes for many aeons.’
I suggested that these ideas would surprise many biologists, and geneticists, who were fixated on the idea of genes being handed down in a simple, vertical, way from parents to offspring.
‘You just need some scaffold to begin your thinking. Then the more you learn the more you realise that the exceptions are almost the rule.’
I was eager to extrapolate this line of reasoning to what really interested me at this stage. ‘The popular conception of a virus is something necessarily nasty, something that infects people and makes them ill – sometimes kills them. But can you conceive that viruses in nature might also have a symbiotic role with animals?’
I was well aware in asking this question that, as early as 1952, Lederberg had published a landmark paper under the title, “Cell genetics and hereditary symbiosis”.5 In this paper he had proposed a new scientific term, the “plasmid”, to cover all sorts of hereditary packages that crossed the genetic divide between different life forms. In this same paper, he stated outright that plasmids were symbiotic organisms that formed part of the genetic inheritance of the life form to which they contributed this new genetic information. From my perspective, this transfer of pre-evolved genetic information was quite different, from an evolutionary perspective, to the Darwinian concept of random changes in the coding sequences of genes arising through errors in copying DNA when cells divided.
He said: ‘It’s a very interesting question.’
We talked about how viruses could change the behaviour and internal chemistry of bacteria, for example by making them resistant to antibiotics. The diphtheria bacterium produced a poison, known as a toxin, which was entirely dependent on the presence of a virus within the bacterium.
So it was that our conversation moved round a topic that we both recognised as extremely important, if potentially very controversial.
I explained what I had learnt from the scientists investigating the hantavirus epidemic, for example the fact that baby deer mice are born without the virus. They acquired it as weanlings, from copious secretions of the virus in the urine and other excreta of the mother. Yet when they acquired this virus, which was so horribly lethal to people, they showed no sign of illness. It was as if, in first meeting the virus when their immune systems were just coming to recognise self from alien, they came to regard the virus as self. In fact, some of the biologists working on the virus-mouse interaction had the feeling that the baby mice grew bigger, stronger, as a result of the presence of the virus. I took a breath and asked the question that had preoccupied my thoughts for the last two months.
‘I know that viruses don’t think. They don’t have a concept of good or bad – they’re not just immoral but amoral. But is it possible a virus could have a beneficial effect on an animal species?’ I should have known better than to use the word “beneficial”, since it is loaded with anthropomorphic overtones. What I meant, and should have asked, was if the presence of a virus might help the host survive.
‘Well, that would be interesting … I don’t know of a clear example of any such mutualistic advantage, but it’s on the cards. And if nothing else, cross-immunity to other infecting agents is certainly going to come into the picture. But I just don’t happen to have it at my fingertips for animals.’
I pushed it a little further. ‘I find myself asking the question, could a viral infection in a species change that species – could it go so far as to create a new species?’
It was probably the most challenging question I put to him, and it resulted in another of those telling pauses.
‘I can commend a book to you that has just come out. It answers the somewhat larger questions. It is by Jan Sapp and it covers symbiosis – the history of the concept.6 Jan is a historian of science from York University, in Canada. He was a visiting scholar here in my laboratory when he wrote the book. He’s been following the thinking of Lynn Margulis, who is probably the most articulate person on this line of thinking. You might have seen something of her writings. Where symbiosis leads to the convergence of two genomes from disparate sources, making, if you like, a very wide hybrid, it becomes the source of evolutionary change of the most major implications. There is a fair consensus now that this is how the eukaryotic cell evolved.’
The eukaryotic cell is a cell with a nucleus. The evolution of such a cell from humble bacterial forebears gave rise to all of the animals, plants, fungi, algae and smaller creatures, such as the amoebae of my school biology days. That same evolutionary step had been extolled by the eminent Darwinian, Ernst Mayr, as the single most important step in the evolution of life. If my interview with Terry Yates had first opened my eyes to the possibility of a new vision of viruses and their role in evolution, this interview with Joshua Lederberg had further encouraged that vision. I left New York more determined than ever to examine it further.
In the opening chapter I outlined a three-way symbiotic relationship between the sea slug Elysia chlorotica, its host alga, and an unknown, virus, putatively a retrovirus, that has entered into a persistent relationship with the slug. But back in 1994 I knew nothing about Elysia, and its relationship with the virus was poorly understood. The truth is that I was in the dark as far as symbiosis was concerned. I had no idea how this biological condition called symbiosis was defined. Did symbiosis imply a different evolutionary mechanism from the highly respected modern Darwinism? My conversation with Lederberg suggested that there were important differences between the two evolutionary disciplines, yet there was no hint that he felt these differences negated the conventional viewpoint. I was mindful of his words of advice: ‘You just need some scaffold to begin your thinking.’ My scaffold would be the biological discipline of symbiosis, and its many examples and operative mechanisms, focusing in particular on how symbiologists – the people who study symbiosis – figured that symbiosis operated as an evolutionary force.
Readers of Jan Sapp’s landmark history of symbiosis will discover how, in 1868, some nine years after Darwin had published The Origin of Species, a Swiss botanist, Simon Schwendener, made a curious discovery about the biological nature of lichens. We are familiar with lichens as the flat, pastel-shaded growths that decorate tombstones or the historic boulders of Stonehenge, but they are far more varied and ubiquitous than the cursory familiarity would suggest. They play an important role in the world’s ecology as pioneer organisms, thriving in inclement environments, such as sand-dunes or the windswept valleys of Antarctica, where they eke out a living on the exposed surfaces, breaking stone down into soil, or soaking up useful reservoirs of water from ambient dew or fog in forest ecologies. In this way, lichens create specialised ecosystems from which other life forms can benefit, for example the hardy growths that endure beneath the Arctic snow providing the main food source for the Sami’s reindeer. At the time of Schwendener’s discovery, lichens had only recently been slotted into place on the biological tree of life as a branch, in the jargon a “class”, of their own coming off the main trunk, or “kingdom”, of the plants, with naturalists devoting their time and energies to defining more than a thousand species that formed the twigs and leaves of that branch. Now, all of a sudden, such endeavour and certainty was thrown to the four winds when Schwendener demonstrated that lichens were not individual organisms at all but intimate associations
