Although it is possible to construct a tree from the concatenated sequences of a small number of highly conserved genes that are found in all organisms, this tree is not representative of the majority of the genes in most genomes. If HGT is frequent, the traditional picture of the tree of life is no longer valid. In this paper, we ask if HGT is on average beneficial to the organism and whether selection will act to increase or decrease its rate. Therefore, cells can potentially evolve to increase or decrease their rate of acceptance of horizontally acquired genes. The gain of a gene by HGT depends on many processes inside the receiving cell. HGT is a risky evolutionary strategy, whereas vertical inheritance is safe because the genes have been tried and tested in the parent. Although there is the potential to gain useful new genes by HGT, there is also the possibility of acquiring useless or harmful genes. In contrast, if a gene is acquired horizontally, there is no guarantee that it increased the fitness of the previous individual. It is therefore clear that vertical inheritance of genes allows natural selection to occur. Hence, the frequency of the beneficial gene will increase in the population. According to the principle of natural selection, if a gene increases the fitness of an individual, that individual will have a larger number of offspring on average, and the offspring will inherit the beneficial gene. Since complete genomes have become available, it has become clear that, in addition to vertical inheritance, there is a substantial rate of horizontal gene transfer (HGT) from unrelated individuals, at least in prokaryotes. Traditionally, genetics is the study of vertical transmission of genes from parents to offspring. The model therefore passes through a Darwinian Threshold. By clustering genomes based on gene content, we show that there are no separate lineages of organisms when the rate of HGT is high however, as the rate of HGT decreases, a tree-like structure emerges with well-defined lineages. In the model, natural selection leads to gradual improvement of the replication accuracy and gradual decrease in the optimal rate of HGT. Modern cells should therefore evolve to reduce HGT if they can, although the prevalence of independently replicating mobile elements and viruses may mean that cells cannot avoid HGT in practice. In contrast, if the gene loss rate is lower, as in modern prokaryotes, then HGT is, on average, unfavourable. HGT leads to the rapid spread of new genes and allows the build-up of larger, fitter genomes than could be achieved by purely vertical inheritance. We show that if rate of gene loss during genome replication is high, as was probably the case in the earliest genomes before the time of the last universal common ancestor, then a high rate of HGT is favourable. We study a model for genome evolution that incorporates both beneficial and detrimental effects of HGT. This phenomenon has been called the Darwinian Threshold. Evolution would then become more tree-like. Only when the HGT rate began to fall, would lineages begin to emerge with their own distinct sets of genes. It has been proposed that the rate of HGT was very high in the early stages of prokaryotic evolution, and hence there were no separate lineages of organisms. If the balance of these effects is beneficial on average, we would expect cells to evolve high rates of acceptance of horizontally transferred genes, whereas if it is detrimental, cells should reduce the rate of HGT as far as possible. Horizontal Gene Transfer (HGT) is beneficial to a cell if the acquired gene confers a useful function, but is detrimental if the gene has no function, if it is incompatible with existing genes, or if it is a selfishly replicating mobile element.
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