A Synergism between Adaptive Effects and Evolvability Drives Whole Genome Duplication to Fixation

作者:Cuypers Thomas D*; Hogeweg Paulien
来源:PLoS Computational Biology, 2014, 10(4): e1003547.
DOI:10.1371/journal.pcbi.1003547

摘要

Whole genome duplication has shaped eukaryotic evolutionary history and has been associated with drastic environmental change and species radiation. While the most common fate of WGD duplicates is a return to single copy, retained duplicates have been found enriched for highly interacting genes. This pattern has been explained by a neutral process of subfunctionalization and more recently, dosage balance selection. However, much about the relationship between environmental change, WGD and adaptation remains unknown. Here, we study the duplicate retention pattern postWGD, by letting virtual cells adapt to environmental changes. The virtual cells have structured genomes that encode a regulatory network and simple metabolism. Populations are under selection for homeostasis and evolve by point mutations, small indels and WGD. After populations had initially adapted fully to fluctuating resource conditions re-adaptation to a broad range of novel environments was studied by tracking mutations in the line of descent. WGD was established in a minority (approximate to 30%) of lineages, yet, these were significantly more successful at re-adaptation. Unexpectedly, WGD lineages conserved more seemingly redundant genes, yet had higher per gene mutation rates. While WGD duplicates of all functional classes were significantly over-retained compared to a model of neutral losses, duplicate retention was clearly biased towards highly connected TFs. Importantly, no subfunctionalization occurred in conserved pairs, strongly suggesting that dosage balance shaped retention. Meanwhile, singles diverged significantly. WGD, therefore, is a powerful mechanism to cope with environmental change, allowing conservation of a core machinery, while adapting the peripheral network to accommodate change. Author Summary The evolution of eukaryotes is characterized by drastic changes in their genome content. Genome expansions have often occurred by duplication of the entire genome. It is generally not know whether organisms gain any adaptive advantage from these mutations. However, they appear to become fixed in response to environmental change. Many interesting whole genome duplications happened long ago in eukaryotic evolutionary history during periods of turbulent genome and species evolution. Genomic data analysis alone cannot resolve the evolutionary mechanisms and consequences of whole genome duplication. Here, we modeled evolution with whole genome duplications in a Virtual Cell model. Simulating populations that undergo a range of different environmental changes we found that next to often increasing fitness directly, whole genome duplications made lineages more evolvable and hence more able to adapt to harsh new environments. Although most duplicates are deleted in subsequent evolution, genes with many interaction partners were retained preferentially, increasing regulatory complexity. Interestingly however, we found that innovation happened most likely in the more loosely connected and less essential genes.

  • 出版日期2014-4