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

Amanda L. Grusz, Michael D. Windham, Kathryn T. Picard, Kathleen M. Pryer, Eric Schuettpelz, Christopher H. Haufler

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish (US)
Pages (from-to)263-283
Number of pages21
JournalAmerican journal of botany
Volume108
Issue number2
DOIs
StatePublished - Feb 2021
Externally publishedYes

Bibliographical note

Funding Information:
We are grateful for financial support from the National Museum of Natural History (Research Grant to A.L.G., M.D.W., and E.S.), the National Science Foundation (DEB‐1907294 to K.T.P.), and for generous startup funding provided by the Swenson College of Science and Engineering at the University of Minnesota Duluth. We also thank the editors and reviewers for their helpful comments and suggestions. This contribution provided respite to A.L.G. during the spring 2020 outbreak of SARS‐CoV‐2; she is especially thankful to her coauthors and colleagues for their company, conversations, and many contributions.

Publisher Copyright:
© 2021 Botanical Society of America

Keywords

  • Döpp-Manton sporogenesis
  • agamospory
  • apogamy
  • asexual
  • diplospory
  • meiotic obligate apogamy
  • premeiotic endomitosis

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