Frozen Evolution. Or, that’s not the way it is, Mr. Darwin. A Farewell to Selfish Gene.

Gene flow, which consists inthe transfer of genes between populations, most commonly via migrating individuals, is an important factor in evolution. Depending on its intensity and on the structure of the population, it can either speed up evolution, or, on the contrary, slow it down significantly. Gene flow becomes an important factor in mobile organisms as well as in organisms that never move during their lifetimes, i.e. also in sessile animals and in plants. This is because, for the purposes  of gene flow, the most important parameter is not based on an individual’s mobility within the population of its species, but rather the ability to migrate, i.e., the usual distance between the place where a particular individual is born and where its offspring are born. Consequently, a pine-tree population whose pollen is spread over large distances by wind has a much greater migration ability, and thus also much more intense gene flow, than a bat population, whose members fly thousands of kilometers in their lifetime, but ultimately breed in the same cave as that in which they were born. It should be mentioned that, in single-cell organisms, especially prokaryotic organisms, the gene flow between populations can take the form of transfer of the genes themselves, such as in a viral transfection. Analogical processes of horizontal gene transfer between individuals of the same species, as well as between different species, can also occur in multicellular organisms. In this case, however, the mobility of individuals tends to be much higher than the mobility of the genes or viruses, rendering these processes practically negligible in gene flow.

While, within a metapopulation, evolutionary novelties arise primarily frommutation processes, gene flow is a much more likely within a population and is therefore more important source of novelties, such as mutated alleles. The incidence of migrants is usually much higher than the frequency of mutations in a population, with each migrant contributing his entire genome, i.e. a large number of alleles that may differ significantly from the alleles present in that population.

While the impact of gene flow is clearly positive in that it helps to maintain genetic polymorphism and thus also the ability of the local population to optimally respond to changes in the environment, from the perspective of the population’s ability to adapt optimally to long-term stable conditions in a given environment, its impact is rather negative. Microevolutionary adaptation of the population to local conditions is achieved by fine-tuning the frequency of the alleles in the population’s gene pool. The frequency of the alleles introduced into local population’s gene pool by migrants equals that of the surrounding populations, which constantly tips the composition of the local population’s gene pool off its optimal value. 

It has been observed, for example, that a relatively isolated blue tit population living in the evergreen forests of Corsica nests later than the tit population on the continent, a beneficial behaviour in that particular environment because it ensures that the time of feeding the offspring coincides with the peak insect levels in the evergreen forests. On the other hand, a minority tit population living in the evergreen forests on the continent nests earlier, simultaneously with the tit populations living in the surrounding dominant deciduous forests, which makes the timing of feeding its offspring inconvenient in relation to insect rates in the relevant locations. It is assumed that gene flow from the surrounding populations prevents the populations on the continent from adapting optimally to the conditions of their local environment (Dias & Blondel 1996).

Gene flow and mutation processes as two sources of evolutionary novelties do not differ only in quantity. While an evolutionary novelty arising from mutation is harmful for its bearer in the absolute majority of cases, novelties acquired through migrants have already passed the natural selection test in another population and are therefore much more likely to be useful or at least selectively neutral. 

Genetic drift is one of the most important mechanisms contributing to changes in the composition of a population’s gene pool. If a population disintegrates into several partial populations isolated in terms of reproduction, the drift effect gradually changes the frequency of alleles in each of these populations. As genetic drift is a stochastic process, allele frequencies in the populations move in different directions. A mathematical model of the genetic drift suggests that genetic diversification should occur very rapidly in populations. However, studies of real populations of the most varied animal and plant species have shown that the frequencies of alleles that can, for some reason, be considered selectively neutral are, in fact, very similar in different populations (Lewontin 1974). It can be demonstrated that the uniformity of selectively neutral alleles within a metapopulation is most likely to be the result of gene flow. Calculations show that even a surprisingly small number of migrants can prevent subpopulations from diversifying genetically through genetic drift (Wright 1931). If we take two populations, each with size N, with an average frequency of the various gene alleles equal to p, subject only to the effects of genetic drift, not selection, and exchanging a certain share m of their genes via migrants in each generation, then the average difference d in the frequencies of the relevant alleles between the populations, or more precisely its absolute value, can be calculated as follows:   

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For example, if we take populations of 10 000 individuals that exchange 10 individuals in one generation (m= 0.001) and that had an initial average allele frequency of 0.5 then, at equilibrium, the average difference in allele frequencies will equal 0.156. As m in the equation represents the ratio of the number of migrants to the population size, then Nm term is equal to the absolute number of migrants and the effects of gene flow consequently do not depend on the size of the population but only on the absolute number of migrants per generation. It follows that, in terms of neutralization of the impact of genetic drift, the same number of migrants will have a comparably strong effect on a population of 10 thousand and on a population of 10 million. Although this number will introduce a relatively smaller share of foreign genes into a large population, genetic drift in this population is also proportionally slower than in a small population. 

As early as in 1931, Sewal Wright deduced that the exchange of 1-2 migrants between partial subpopulations can prevent genetic differentiation and thus speciation of subpopulations within a metapopulation as a result of genetic drift and will ensure that the metapopulation develops synchronously as a single evolutionary unit (Fisher 1958). This conclusion has also been verified experimentally, for example, by studies of differentiation in red flour beetle populations (Schamber & Muir 2001).

Calculations show that, if the diversification of subpopulations is the result of natural selection and not genetic drift, the number of migrants required to maintain the genetic cohesion of the metapopulation is substantially higher (Gavrilets 2000; Rieseberg & Burke 2001). If a dominant allele is being eliminated in a given local subpopulation by natural selection with intensity s, i.e. at the rate of ps per generation (p corresponds to the frequency of the allele in the subpopulation, s – selection coefficient) and, at the same time, it enters that subpopulation via gene flow at a rate of  (P – p)m from surrounding subpopulations (P corresponds to the frequency of the allele in the surrounding subpopulations, m – the intensity of gene flow), any particular ratio of the selection and gene flow intensity can ultimately result in a balanced frequency of the given allele in the subpopulation

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If selection is much stronger than gene flow, the allele can practically disappear from the local subpopulation and, analogously, if gene flow is much stronger than selection, the frequency of the allele in the local subpopulation can very closely resemble its frequency in the surrounding subpopulations.

The intensity of gene flows detected in real populations is so high that, even in the case of plants, a useful allele can spread quite rapidly to all the subpopulations within the whole range of the given species, allowing the species to behave as an evolutionary unit in terms of adaptive evolution. Subpopulations tend to differ in non-adaptive traits or in traits expressing low additive heritability that are difficult to select (Rieseberg & Burke 2001).