Freeling and Thomas (28
) have suggested that the duplication and retention of duplicate regulatory factors following polyploidization could contribute to an increase in complexity during the evolution of multicellular organisms. Whether such increase in complexity has occurred during evolution has been a topic of debate for some time. The resistance to this idea comes from the idea of “progress” in evolution, which is unlikely to occur. It is important to realize however that “progress” and “complexity” are not necessarily synonymous. The new suggestion is that complexity is driven by degenerative processes, such as mutation and deletion, following polyploidization events within the context of regulatory balance and selection. This proliferation of regulatory functions can foster greater complexity.
New variation in life comes from mutations and new genes from duplications. Numerous examples are known of proliferation of genes by tandem duplication and divergence. Accumulation of mutations in one copy of the duplicate results in divergence to a new function, which is referred to as neofunctionalization. Alternatively, the two copies could diverge such that each member of the pair performs separate aspects of the original function, which is called subfunctionalization (31
One explanation for the retention of duplicate regulatory genes during diploidization might be that sub or neo functionalization (i. e. altered tissue specific expression or enzymatic action) has occurred for one member of the duplicate pair so that deletion of either copy removes a required function from the genotype which would be detrimental and thus selected against. To some degree, this almost certainly occurs, but the evidence for purifying selection against mutation accumulation for the retained classes of genes suggests otherwise for many genes (10
). Sub and neo functionalization of duplicates is apparently a slower process than once thought. As pointed out by Freeling and Thomas (28
), maintenance of balance of the regulators is required immediately upon polyploidization and deletion of one member of a pair is predicted to have detrimental consequences.
Therefore, one might envision the following scenario. The duplication of the genome would increase the copy number of all genes. Regulatory factors are present in a balanced stoichiometry that makes them resistant to loss. The retention over long evolutionary time makes them available for potential mutational change that could lead to sub and neo functionalization. However, in order for this to happen, they must escape from the balanced stoichiometry. One might imagine that one way in which this could happen might be by the deletion of specific target genes. This must occur in such a manner that only some targets of a balanced regulatory system are removed at a time so that a detrimental situation is not created. As a gradual deletion of multiple targets accumulate, selection pressure might occur to shift a regulatory balance. Another possibility might be the occurrence of cis-dominant regulatory lesions in critical target loci that would alter their expression in such a manner to allow a shift in the balance of regulators (). It is certain, however, that, in order for whole genome duplication to contribute to an increase in complexity, divergence of duplicate regulators must occur at some point following the various rounds of polyploidization and diploidization during plant evolution.
The principle proposed by Freeling and Thomas (28
) is that with multiple whole genome duplication events in the history of angiosperms, there has been a continual proliferation of regulatory genes. They are held in the evolutionary lineage against deletion because of their balance property. As a new balance is eventually found and divergence occurs, developmental and metabolic processes will become more complex. Thus, on this hypothesis, complexity is driven at least in part by the cycle of polyploidization and diploidization followed by random degenerative mechanisms (deletion and mutations) that do not invoke “progress”.