Ecophysiological differentiation between life stages in filmy ferns (Hymenophyllaceae)

Abstract

Desiccation tolerance was a key trait that allowed plants to colonize land. However, little is known about the transition from desiccation tolerant non-vascular plants to desiccation sensitive vascular ones. Filmy ferns (Hymenophyllaceae) represent a useful system to investigate how water-stress strategies differ between non-vascular and vascular stages within a single organism because they have vascularized sporophytes and nonvascular gametophytes that are each capable of varying degrees of desiccation tolerance. To explore this, we surveyed sporophytes and gametophytes of 19 species (22 taxa including varieties) of filmy ferns on Moorea (French Polynesia) and used chlorophyll fluorescence to measure desiccation tolerance and light responses. We conducted phylogenetically informed analyses to identify differences in physiology between life stages and growth habits. Gametophytes had similar or less desiccation tolerance (ability to recover from 2 days desiccation at − 86 MPa) and lower photosynthetic optima (maximum electron transport rate of photosystem II and light level at 95% of that rate) than sporophytes. Epiphytes were more tolerant of desiccation than terrestrial species in both life stages. Despite their lack of greater physiological tolerances, gametophytes of several species occurred over a wider elevational range than conspecific sporophytes. Our results demonstrate that filmy fern gametophytes and sporophytes differ in their physiology and niche requirements, and point to the importance of microhabitat in shaping the evolution of water-use strategies in vascular plants.

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Fig. 1

Photographs by J. H. Nitta

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Acknowledgements

Members of the Davis Lab and Jonathan Losos provided helpful discussion and comments on drafts. Saad Amer, Ravahere Taputuarai, Tohei Theophilus, and Suzanne Vinnette assisted with fieldwork and experiments. Weston Testo provided advice on settings for the DT test. James M. R. Brock and an anonymous reviewer provided feedback that improved the manuscript. Staff at the University of California Berkeley’s Richard B. Gump South Pacific Research Station, Moorea, French Polynesia, in particular Valentine Brotherson, Neil Davies, Hinano Teavai-Murphy, and Frank Murphy, provided logistical support for fieldwork. Funding provided in part by the National Science Foundation (Doctoral Dissertation Improvement Grant DEB-1311169 to JHN and CCD), Setup Funds from Harvard University to CCD, American Society of Plant Taxonomists (Research Grant for Graduate Students to JHN), Garden Club of America (Award in Tropical Botany to JHN), Harvard University Herbaria (Fernald Fieldwork Fellowship to JHN), Society of Systematic Biologists (Graduate Student Research Award to JHN), and Systematics Association (Systematics Research Fund to JHN).

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JHN conceived of and designed the study with input from JEW, NMH, and CCD. Data collection was performed by JHN and TWW. Data analysis was performed by JHN. The first draft of the manuscript was written by JHN, with subsequent comments and edits from the other authors. All authors read and approved the final manuscript.

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Correspondence to Joel H. Nitta.

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Nitta, J.H., Watkins, J.E., Holbrook, N.M. et al. Ecophysiological differentiation between life stages in filmy ferns (Hymenophyllaceae). J Plant Res (2021). https://doi.org/10.1007/s10265-021-01318-z

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Keywords

  • Chlorophyll fluorescence
  • Desiccation tolerance
  • DNA barcoding
  • French Polynesia
  • Gametophyte
  • Hymenophyllaceae