Gene duplications potentiate adaptive evolution of complex traits

Matthew Moreno, Cameron Haynes , Charles Ofria, Alexander Lalejini , Luis Zaman

Much of extant genetic material is known to have resulted from earlier genetic duplications. On this basis, gene duplications are widely recognized as a key factor in the evolution of organismal complexity --- both in producing novel adaptations (i.e., neofunctionalization) and in accumulating functional specialization (i.e., subfunctionalization). However, across the tree of life, no ready counterfactual exists to directly test the aggregate impact of gene duplication on complexity over long evolutionary timescales.
To this end, we turn to the Avida platform, using digital experiments to investigate two questions in specific:
(1) Does gene duplication boost evolved (a) structural and (b) functional complexity?
(2) If so, does evolved complexity rely on duplicated genetic information (i.e., versus simple genome expansion alone)?
As to (1): we find clear evidence that duplicative inserts yield virtual organisms with higher complexity, in both measures. However, the causal role of genetic information differed between measures of complexity. Regarding (a) structural complexity: duplications grew genome size, on average, larger than randomized and empty-insert controls. By contrast, though, duplicated genetic information more weakly affected coding-site structure, with complexity here attributable to larger genome size alone. Regarding (b) functional complexity, duplications sped up evolutionary innovation compared to controls. For simple phenotypic traits, faster adaptation was attributable to increased genome size alone. For complex phenotypic traits, however, adaptation depended directly on duplicated genetic information. Such complex traits arose disproportionately from duplicated coding sites, and seldom arose in large-genome-only treatments.
In sum, our findings show that genetic information in duplicative inserts can directly drive genome expansion and complex adaptation, but that simpler adaptations and structural complexity may follow from larger genome size alone. This perspective notably integrates adaptationist and neutralist framings, as duplicated information actively catalyzes complex functionality while certain aspects of structural complexity may instead accrue passively.