The evolution of reproductive leaf dimorphism in two globally distributed fern families is neither stepwise nor irreversible, unless further specialization evolves.

Abstract

A contemporary interpretation of Dollo's Law states that the evolution of a specialized structure is irreversible. Among land plants, reproductive specialization shows a trend toward increasing complexity without reversion, raising questions about evolutionary steps and the irreversibility of reproductive complexity. Ferns exhibit varied reproductive strategies; some are dimorphic (producing separate leaves for photosynthesis and reproduction), while others are monomorphic (where one leaf is used for both photosynthesis and spore dispersal). This diversity provides an opportunity to examine the applicability of Dollo's Law in the evolution of reproductive leaf specialization. We analyzed 118 species in Blechnaceae and Onocleaceae, applying quantitative morphometrics and phylogenetic comparative methods to test the pillars of a modernized interpretation of Dollo's Law. The evolution of dimorphism in Blechnaceae is neither stepwise nor irreversible, with direct transitions from monomorphism to dimorphism, including several reversions. In contrast, Onocleaceae exhibits an irreversibility to monomorphism only upon further specialization of fertile leaves for humidity-driven spore dispersal; this suggests that additional specialization, not dimorphism alone, may facilitate irreversibility. These results provide insight into the canalization of fertile-sterile leaf dimorphism in seed plants, where the addition of traits like heterospory and integuments lead to further specialization and potential irreversibility. These findings suggest that as new specialized traits evolve alongside preexisting ones, reversion may become increasingly unlikely.