The Evolutionary Value of Recombination Is Constrained by Genome Modularity

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Abstract
Genetic recombination is a fundamental evolutionary mechanism promoting biological adaptation. Using engineered recombinants of the small single-stranded DNA plant virus, Maize streak virus (MSV), we experimentally demonstrate that fragments of genetic material only function optimally if they reside within genomes similar to those in which they evolved. The degree of similarity necessary for optimal functionality is correlated with the complexity of intragenomic interaction networks within which genome fragments must function. There is a striking correlation between our experimental results and the types of MSV recombinants that are detectable in nature, indicating that obligatory maintenance of intragenome interaction networks strongly constrains the evolutionary value of recombination for this virus and probably for genomes in general. Genetic exchange between organisms, called recombination, occurs in all biological kingdoms and is also common in viruses in which it may threaten the long-term control of important human pathogens such as HIV and influenza. Although recombination can produce advantageous gene combinations, bioinformatic analyses of bacterial genomes have suggested that recombination is not well tolerated when it involves exchanges of genes that interact with a lot of other genes. Using laboratory-constructed recombinants of a small plant virus called MSV, Martin and co-workers provide the first direct experimental evidence that the evolutionary value of exchanging a genome fragment is constrained by the number of ways in which the fragment interacts with the rest of the genome. They note that fitness losses suffered by artificial MSV recombinants increase with decreasing parental relatedness. Furthermore, these losses accurately anticipate the patterns of genetic exchange detectable in natural MSV recombinants, suggesting that they accurately reflect the impact of deleterious selection on natural isolates of the virus.