Untangling poikilohydry and desiccation tolerance: evolutionary and macroecological drivers in ferns

Abstract

Background and aims: Poikilohydry describes the inability of plants to internally regulate their water content (hydroregulation), whereas desiccation tolerance (DT) refers to the ability to restore normal metabolic functions upon rehydration. The failure to clearly separate these two adaptations has impeded a comprehensive understanding of their unique evolutionary and ecological drivers. Unlike bryophytes and angiosperms, these adaptations in ferns are sometimes uncorrelated, offering a unique opportunity to navigate their intricate interplay.

Methods: We classified ferns into two syndromes: the Hymenophyllum-type (H-type), encompassing species with filmy leaves lacking stomata that experience extreme poikilohydry and varying degrees of DT, and the Pleopeltis-type (P-type), consisting of resurrection plants with variable hydroregulation but high DT.

Key results: The H-type evolved during globally cool Icehouse periods, as an adaptation to low light levels in damp, shady habitats, and currently prevails in wet environments. Conversely, the P-type evolved predominantly under Greenhouse periods as an adaptation to periodic water shortage, with most extant species thriving in warm, seasonally dry habitats.

Conclusions: Out study underscores the fundamental differences between poikilohydry and DT, emphasizing the imperative to meticulously differentiate and qualify the strength of each strategy as well as their interactions, as a basis for understanding the genetic and evolutionary background of these ecologically crucial adaptations.

Keywords: Abiotic stress; dehydration; drought; homoiohydry; resurrection plants; water loss.