Darwinian theory proposes an essentially linear pattern of evolution, with new species arising through branching divergence from ancestral stock, symbiosis involves a reticulate pattern of evolution through the partnership of different life forms, from species to whole kingdoms. On the face of it this would appear to suggest that symbiogenesis and Modern Darwinism have little in common. But this is not the case. In spite of the clear and important differences between the evolutionary mechanics that underlie the two evolutionary paradigms, symbiosis does not contradict evolutionary theory and it does not contradict Darwin’s concept of natural selection in particular. The crucial question we need to ask ourselves is not whether natural selection applies to the evolution of symbiotic relationships but rather how exactly it operates in circumstances where different life forms interact at a biologically meaningful level.
To put it bluntly – is there something different about the way in which natural selection works in symbiogenesis as opposed to mutation-plus-selection? Let us examine two familiar examples of symbiotic partnerships, and see if we can determine the answer.
Hummingbirds are native to the warmer parts of the Americas, where more than three hundred species depend on the nectar of flowers for their daily sustenance. The birds’ wings have been highly adapted by natural selection to allow them to hover, with pinpoint accuracy, over the flower, and their beaks have also become exceptionally long and shaped to fit the flower head, while their elongated tongues reach down into the well of nectar at the very bottom of the flower. Meanwhile, the flower has also been adapted to fit the bill of the hummingbird. One of the most striking examples of these birds is the violet sabrewing, which has a curved bill that fits the floral tube of its partner, the columnia flower, as accurately as a scimitar fits its streamlined scabbard. The precise match of bill and flower is important, since it deepens and strengthens the partnership, making it more likely that only the sabrewing will feed from the columnia, while the columnia’s stamens are positioned to dab pollen on exactly the right point of the bird’s forehead, so that it fertilises the next flower it visits. From this mutualistic symbiosis it is clear that selection is operating to a significant degree at the level of the partnership, stabilising and making permanent the living interaction.
If we turn our attentions to the behavioural symbioses of the cleaner stations, once again we see that these involve important changes in behaviour for both predators and cleaners: the predators put aside hunger and aggression, while the cleaner fish and tiny shrimps put aside fear and the instinct to flee. Such dramatic changes of behaviour in predator and potential prey would have to be hardwired into the genomes of the interacting partners and, just as we have seen with the hummingbirds and their floral partners, this involves each of the partners changing its behaviour in relation to the other. Once again we see selection operating at the level of the partnership in a mutualistic symbiosis. This also raises important questions about the real nature of viruses and their hosts. Could it be that selection might also be operating at the level of the virus-host interaction? If so, at what stage in the interaction did selection switch from operating at selfish, individual, even selfish gene, level, to recognise and begin to operate at this profoundly important level? This very question was addressed by the eminent evolutionary biologist, John Maynard Smith, late professor at the University of Sussex, and widely acclaimed as a pioneering Modern Darwinian.
In a chapter in the multi-authored book, Symbiosis as a Source of Evolutionary Innovation, which was edited by Lynn Margulis and René Fester, Maynard Smith developed a very interesting extrapolation of the Darwinian view of symbiosis. Believing that symbiosis played an important part in three of the five major transitions of life, he nevertheless insisted that there was no reason for symbiosis to challenge the neo-Darwinian view of evolution. But he also believed that, in order to accommodate the partnership aspects of symbiosis, there were circumstances in which natural selection must operate at a different level in symbiosis when compared with how it operates in the many Darwinian extrapolations.
It was even more helpful when, in exploring this further, he examined symbioses involving a microbial symbiont and a more complex host, and these he divided into various sub-categories. Where the symbiont could survive and reproduce independently of the host, this would suggest an evolution along conventional “selfish” Darwinian lines. But where the symbiont cannot survive without the host, and most particularly where the symbiont is dependent on the host for reproduction – a condition Maynard Smith termed “direct transmission” – the role of natural selection would inevitably change. Viruses can never survive, or reproduce, without their hosts. In this respect, viruses are said to be obligate parasites, so we should not be too surprised to discover that Maynard Smith included viruses in his discussion of symbionts that were only capable of reproduction through direct transmission.
In his words:
With direct transmission, the genes of the symbiont will leave descendants only to the extent that the host survives and reproduces. In general, therefore, mutations in the genes of the symbiont will be established by selection only if they increase the fitness of the host.9
When he writes that “mutations … will be established by selection”, he is referring to evolution taking place in the conventional Darwinian sense. Or to put it simply, the symbiont – the virus in virus-host interactions – will only be honed by mutation-plus-selection in a manner that increases the fitness of the host. In other words, the virus is now responding to the presence, and needs, of its symbiotic partner.
This interpretation of symbiosis, as seen from a Darwinian perspective, provides an important measure of common ground between the two disciplines. As we have seen in the examples of the hummingbirds and the cleaner stations, a symbiologist might adopt a slightly different perspective, regarding both host and parasite as symbionts, so that, rather than merely looking at the relationship from a single perspective, the symbiologist would examine how this might apply to the partnership. And all the evidence from what is now a weighty world of symbiology, with its study of a vast array of such partnerships, would imply that in microbe-host partnerships each of the partners responds to the presence of the other – or to put it from an evolutionary perspective, selection will be seen to operate, to a significant degree, at the level of the partnership. This perspective is seen to operate throughout all the levels of symbiosis, and, in the evolutionary sense, to symbiogenesis, whether at behavioural, metabolic or genetic level.
Within the genetic symbioses, there are examples of sudden and major change, where the genomes of radically different life forms unite to form a single novel, holobiontic, genome.10 In this very dramatic situation, which has the potential to give rise to very rapid evolutionary change, it is inevitable that selection will operate, to significant degree, at the level of the new holobiontic genome. It is perhaps not altogether surprising that some biologists see an irrevocable chasm in the evolutionary dynamics of this most powerful of genetic symbiosis and the gradualism that is assumed to be central to Darwinian evolution. But Maynard Smith does not agree. He goes on to emphasise that there is no contradiction between Darwin’s belief that complex adaptations arise by the natural selection of numerous intermediates, and the possibility that new evolutionary potentialities may arise suddenly if genetic material that has been programmed by selection in different ancestral lineages is brought together by symbiosis.
This is important not only in offering the potential of reconciling the dynamics of Darwinian and symbiotic evolution, but also in interpreting the role of symbiotic viruses in our human evolution.
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