Epigenetic resolution of the 'curse of complexity' in adaptive evolution of complex traits.

The age of most genes exceeds the longevity of their genomic and physiological associations by many orders of magnitude. Such transient contexts modulate the expression of ancient genes to produce currently appropriate and often highly distinct developmental and functional outcomes. The efficacy of such adaptive modulation is diminished by the high dimensionality of complex organisms and associated vast areas of neutrality in their genotypic and developmental networks (and, thus, weak natural selection). Here I explore whether epigenetic effects facilitate adaptive modulation of complex phenotypes by effectively reducing the dimensionality of their deterministic networks and thus delineating their developmental and evolutionary trajectories even under weak selection. Epigenetic effects that link unconnected or widely dispersed elements of genotype space in ecologically relevant time could account for the rapid appearance of functionally integrated adaptive modifications. On an organismal time scale, conceptually similar processes occur during recurrent epigenetic reprogramming of somatic stem cells to produce, recurrently and reversibly, a bewildering array of differentiated and persistent cell lineages, all sharing identical genomic sequences despite strongly distinct phenotypes. I discuss whether close dependency of onset, scope and duration of epigenetic effects on cellular and genomic context in stem cells could provide insights into contingent modulation of conserved genomic material on a much longer evolutionary time scale. I review potential empirical examples of epigenetic bridges that reduce phenotype dimensionality and accomplish rapid adaptive modulation in the evolution of novelties, expression of behavioural types, and stress-induced ossification schedules.