Evolution of complex phenotypes through successions of adaptive steps
Tin Y. Pang, Martin Lercher

The emergence of complex phenotype is a fascinating question of evolutionary biology, and we sought to understand preadaptation which facilitated the development of complex phenotypes, in the context of bacterial metabolic network. Genes coordinated for a phenotype are likely to cluster on the same place of the genome, which so allows horizontal gene transfer (HGT) to pass the phenotype to another bacterium. But for a complex phenotype, its genes are clustered on different places of the genome cannot be transferred adaptively; it is preadaptation, which refers to adaptive transfer of a segment relevant to a complex phenotype for other purposes, that allows it later to be recruited for the complex phenotype. To search for preadaptation in the evolutionary history of E. coli, we reconstructed the ancestral genomes from various strains, identified the transferred genes, grouped them into possible transferred segments, and analyzed the gains in nutritional phenotypes corresponding to the acquisitions of segments of metabolic genes. Properties of these HGT segments inferred from data are enumerated and compared with a model of HGT, which shows that: 1) HGT segments are likely to adaptive, and segments carrying reactions essential to phenotypic gains but non-adaptive are rare; 2) the landscape of segment transfer for complex phenotypes is directional and path-dependent; 3) cooperation between HGT segments to support various nutritional phenotypes are observed to be more frequent than expected, which serves as an evidence to preadaptation in the evolution of bacterial metabolic network.