A drought-driven model for the evolution of obligate apomixis in ferns: evidence from pellaeids (Pteridaceae)

Premise: Xeric environments impose major constraints on the fern life cycle, yet many lineages overcome these limitations by evolving apomixis. Here, we synthesize studies of apomixis in ferns and present an evidence-based model for the evolution and establishment of this reproductive strategy, focusing on genetic and environmental factors associated with its two defining traits: the production of “unreduced” spores (n = 2n) and the initiation of sporophytes from gametophyte tissue (i.e., diplospory and apogamy, respectively). Methods: We evaluated existing literature in light of the hypothesis that abiotic characteristics of desert environments (e.g., extreme diurnal temperature fluctuations, high light intensity, and water limitation) drive the evolution of obligate apomixis. Pellaeid ferns (Cheilanthoideae: Pteridaceae) were examined in detail, as an illustrative example. We reconstructed a plastid (rbcL, trnG–trnR, atpA) phylogeny for the clade and mapped reproductive mode (sexual versus apomictic) and ploidy across the resulting tree. Results: Our six-stage model for the evolution of obligate apomixis in ferns emphasizes the role played by drought and associated abiotic conditions in the establishment of this reproductive approach. Furthermore, our updated phylogeny of pellaeid ferns reveals repeated origins of obligate apomixis and shows an increase in the frequency of apomixis, and rarity of sexual reproduction, among taxa inhabiting increasingly dry North American deserts. Conclusions: Our findings reinforce aspects of other evolutionary, physiological, developmental, and omics-based studies, indicating a strong association between abiotic factors and the establishment of obligate apomixis in ferns. Water limitation, in particular, appears critical to establishment of this reproductive mode.