In the last section I treated interactions between microorganisms and multicellular individuals the way biologists usually deal with individuals belonging to the same species: if they continue to engage in fitness-affecting interaction, they constitute a Darwinian population. Unfortunately, this is not the way biologists deal with multi-species communities. I have therefore thrown out the old tradition of thinking about evolutionary phenomena, which, as Bouchard pointed out (2014), focusses on modelling interactions among entities of the same type:
Population approaches usually model the same type of entities at similar levels of organisation (cells with cells, genes with genes, individual organisms with individual organisms, groups with groups). But how are we to model evolving assemblages of motley unrelated parts at different levels of organisation?
I need to say a couple of words, therefore, to explain why a multi-species account of Darwinian population is the proper way to think about ENS and, furthermore, how to understand ENS in diverse populations built of such distinct elements as fungi, bacteria and cats.
If we start with a very basic account of natural selection—i.e. that evolution by natural selection will take place in any population (a group of causally connected objects) in which there are phenotypic variations, heritability, and differences in fitness (reproductive output) caused, at least in part, by these variations—then we have to, at least partially, abandon this tradition, because the consequence of this account is that a lion, a gazelle and a virus belong to the same Darwinian population as long as they continue to engage in causal interactions that influence their reproductive output. Godfrey-Smith (2009) calls these interactions ‘competitive interaction with respect to reproduction’, and denotes them as α (alpha), which defines the extent to which increasing one individual’s fitness reduces another’s in the population under consideration. Alpha is a continuous variable ranging from 0 to 1. The closer it is to 1, the more increasing the fitness of one individual reduces the fitness of others. In the context of the last section, this might be redefined as the extent to which increasing the fitness of a member of the Darwinian population of a given reproducer reduces the fitness of the focal unit, and so it will be understood here. For me, this parameter is a key that enables us to link a group of elements within the Darwinian population of a given reproducer despite their phylogenetic diversity. Let me present two scenarios to demonstrate this.
Suppose there is a chimpanzee that competes with a group of other chimpanzees for a limited number of bananas. Suppose, then, that the banana is a crucial resource that is necessary to survive and reproduce. Suppose as well that other resources, such as sexual mates, etc., are unlimited. Our chimpanzees, therefore, have no problem acquiring resources other than bananas. In such a scenario, therefore, competition would involve just one resource and differences in fitness would mirror differences in acquiring bananas. Suppose that, in a second scenario, a chimpanzee competes with a group of chimpanzees and cats; for both—cats and chimpanzees—bananas are a crucial resource and all other resources are unlimited. Again, therefore, competition would involve just one resource and differences in fitness would mirror differences in acquiring bananas. Cats and chimpanzees that are able to acquire them readily would increase in number over generations, and in the end a particular phenotype of a cat or a chimpanzee (one that knows perfectly well how to get bananas) might outcompete other chimpanzees and cats. These scenarios are, of course, fictional. However, they show an important thing: in both scenarios there is strong competition over resources that leads to the diverse reproduction of individuals. It does not matter whether they belong to the same species or not, because their reproductive output is limited. Their fitness is interdependent: the more offspring I produce, the less you are able to produce; or, as Godfrey-Smith (2009) wrote, ‘a slot I fill in the next generation is a slot that you do not fill’. This might be easily understood when there is a strong competition among conspecifics. However, the same goes for the competition between viruses and cats. Of course, they do not compete for bananas directly like the cats and chimpanzees in the scenario above. For instance, if we were to add viruses to that scenario, then they would compete for bananas as well, but in a more abstract sense. Viruses would try to use certain host resources (such as necessary nutrients that the host has assimilated from bananas) for production of their own offspring. Indeed, viruses would use resources that the host might have used to multiply. Thus, a slot that might be filled by host offspring would be filled instead by viruses.
So far we have been considering only one side of the coin: namely, fitness-affecting interactions with a negative impact on the fitness of the focal unit. However, when we take a reproducer and look for the other reproducers making up its Darwinian population, then we see that it engages as well in interactions exerting a positive impact on fitness. I call these interactions fitness-enhancing. An interesting question is whether their existence is necessary for evolution by natural selection to occur in multispecies Darwinian populations. I think the answer is ‘no’. I think that competitive interactions are more primal and fundamental than enhancing interactions, and that the latter, in fact, evolve in response to the former. As Nowak (2006) put it: ‘The question how natural selection can lead to co-operative behaviour has fascinated evolutionary biologists for several decades’. That said, co-operative interactions are considered much more complex, and a fundamental issue in evolutionary biology is to understand the conditions under which they can evolve from competitive interactions. To give an example of such conditions: in algae, single cells co-operate to form clusters in response to competitive interactions with predatory protists, because this strategy reduces their chance of being eaten (Boraas et al. 1998; Fisher et al. 2016).
In spite of this, I think that for natural selection to occur, competitive interactions with respect to reproduction are sufficient; it is from them that fitness-enhancing interactions derive. In other words, when there is strong competition between Darwinian individuals, some of them might engage in co-operative actions with others in order to enhance their common fitness. This kind of interaction might have a positive influence on the fitness of the focal unit and change the outcome of competitive interactions. Thus, in many cases, the Darwinian population of a given reproducer would comprise individuals exerting both a positive and negative influence on its fitness; the reproductive output of the focal unit would be the result of these two types of interactions. However, they are not necessary, either for the process of natural selection to occur in multispecies populations or for the subsequent parts of this paper; thus, while interactions of this kind are very interesting, I am not going to consider them more deeply.
However, Matthewson (2015), and Godfrey-Smith as well (2009), argued that this is not the whole story (i.e. alpha) and that something more is needed in order to have a population that might undergo natural selection. Building upon Templeton’s (1989) idea of species, Matthewson concluded that a group of individuals engaged in fitness-affecting interactions must be under the influence of mechanisms that sustain their similarity in order to undergo paradigm natural selection. Thus, he argued that we need another parameter, which he called exchangeability and divided into genetic and demographic. The former refers to the ability to combine genes with others in the group, the latter to a situation in which individuals occupy the same niche and thus are under the same selection pressure. These additional mechanisms, if strong, assure that the individuals in question are very similar. Matthewson’s intention in introducing this new parameter was to avoid situations in which a group of individuals is called a Darwinian population simply because they have a high alpha value, when, in fact, they compete over just one crucial resource and have nothing else in common. That’s right: they might be just two different species, occupying niches that, despite one similarity, are completely different. For instance, a chimpanzee and a virus. As a result, he argued, natural selection would not lead to a situation in which fitter individuals take over a niche, as it is hard to imagine a virus taking over a chimpanzee’s niche.
Well, I agree this is true, but, at the same time, I do not think that this is what natural selection is about. Generally, evolution by natural selection concerns causative interactions that lead to differences in the reproductive output of individuals struggling for existence, as I argued above. Of course, very often evolution by natural selection leads to a niche being taken over by fitter individuals. This is the case when there are strong completive interactions among members that exchange genes, as in sexual species in which a fitter allele may become fixed in a gene pool. Sexual reproduction may even be very important, because it ‘speeds up’ the formation of new combinations of alleles, and cumulative adaptation might emerge much faster within such a group of individuals (Morran et al. 2011). However, I don’t think that exchangeability states whether there will be natural selection; rather, it is just another parameter (albeit an important one) indicating what the evolution of a population under consideration would look like. For instance, given a high rate of exchangeability, we might see how one phenotype takes the place of another in a given niche, as when a bacterial strain evolves a new trait that enables it to acquire resources more rapidly and, as a result, outcompete other strains. However, given a low rate of exchangeability, Darwinian selection might still exist on the highest level. For example, during the 1918 flu pandemic the rate of exchangeability between the flu virus and human beings was low; nevertheless, the reproductive output of many people was shaped mainly by interactions with viruses.
Basically, I agree that exchangeability is an important parameter. However, I do not think that it should be placed on the same level in the hierarchy as α, because alpha is the parameter that decides whether or not there is a struggle for existence. If alpha is high, then the individuals in question engage in Darwinian interactions despite their low rate of exchangeability. However, if there is a high rate of exchangeability but very low alpha, then there is no Darwinian selection, but only a group of individuals that are similar because they occupy the same niche and/or can potentially interbreed. Thus, I think that the Darwinian population of an individual is determined by interactions that influence its reproductive output. The stronger these interactions, the more there is a struggle for existence, and the greater the likelihood that a population is Darwinian. Other factors such as exchangeability, fitness enhancing interactions, variance, integration, etc. are secondary characteristics of a Darwinian population that might help us understand how the community in question will evolve.