Evolution in reverse gear: the molecular basis of loss and reversal

Three types of regressive evolution are reviewed: loss, reversal, and regain after loss. Loss refers to the loss of a physical entity, either a structure or an organ, whereas reversals apply to character states returning to plesiomorphic from apomorphic conditions. The regain of characters after their loss represents a third type of evolutionary character change. The reconstruction of multiple losses and gains of characters by mapping on phylogenies is often problematic because of a lack of information about the relative likelihood of losses and gains. A developmental genetic approach using morphological, developmental, and molecular analysis is therefore an extremely important adjunct to phylogenetic approaches in interpreting losses, reversals, and regains. The molecular developmental basis of character loss and reversal is gradually becoming better understood. Loss of organs can occur by gain-of-function mutations (suppression) and loss-of-function mutations (that often leave a vestigial structure). The regain of characters after loss may occur by regulatory capture (a gain-of-function mutation) or by loss of function in suppressor genes. Reversals may occur by cryptic innovation (the formation of a new structure that mimics the old structure by gain-of-function mutations) or by loss of gene function associated with the apomorphic state (although this may have pleitropic or neomorphic effects). The genetic landscape of reversal is illustrated by the reversal to polysymmetry from monosymmetry in flowers. The range of observed phenotypes, loss with vestige, cryptic innovation, and loss with neomorphism matches the range of changes predicted."In plants with separated sexes, the male flowers often have a rudiment of a pistil; and Kolreuter found that by crossing such male plants with an hermaphrodite species, the rudiment of the pistil in the hybrid offspring was much increased in size; and this shows that the rudiment and the perfect pistil are essentially alike in nature" (Darwin 1859).