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

Abstract

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 (≈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.

Selective constraints on coding sequences of nervous system genes are a major determinant of duplicate gene retention in vertebrates

“…Finally, we examined the relation between the level of protein connectivity and retention rates. The number of protein-protein interactions was previously taken as a proxy for sensitivity to dosage imbalance (Prachumwat and Li 2006;Flagel and Wendel 2009;Rodgers-Melnick et al 2013;Cuypers and Hogeweg 2014). We observed that mouse orthologs of zebrafish 3R ohnologs had a significantly higher connectivity than orthologs of singletons ( Figure S11A), in agreement with previous studies (Hakes et al 2007;Liang and Li 2007;Rodgers-Melnick et al 2012).…”

“…On the other hand, whole-genome duplications have often been claimed to be beneficial in the long term, since the addition of new genes to genomes provides new material for evolution to act on, and increases evolvability of the lineages (Cuypers and Hogeweg 2014;Kondrashov 2012;Van de Peer, et al 2009). A particularly interesting example is the ancestral 2R event, which added to the genomes of vertebrates a large number of regulatory genes, such as transcription factors, as an indirect effect of purifying selection for gene dosage balance.…”

Using digital organisms to investigate the effect of whole genome duplication in (artificial) evolution

“…Furthermore, the modular arrangement of duplicated GRNs may also result in functionally redundant modules, contributing to the genetic or mutational robustness at the GRN level. This facilitates the rewiring of novel functional modules without disturbing the ancestral one, a feature that is expected to be especially advantageous under unstable challenging environments (23,36). In this respect, our observations are compatible with previous claims that increased modularity results in increased evolvability (32,(39)(40)(41)(42)(43)(44).…”

Comparative analysis of zebrafish bone morphogenetic proteins 2, 4 and 16: molecular and evolutionary perspectives

“…Similarly to what happens for BMP16, parallel lineagespecific gene losses have been reported for other genes that were present at the base of the vertebrate lineage and have been lost in selected taxa throughout evolution [44][45][46][47]. Gene retention is often associated with adaptive advantages [48,49] and the maintenance of BMP16 in Lepidousaria genomes is most likely due to a selective advantage related to specific traits (e.g. locomotion, reproduction, feeding, adaptation to a particular environment) that the gene confers (see below for our hypothesis of the adaptive advantage promoted by BMP16).…”