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First published online October 14, 2009; doi:10.3732/ajb.0900047 American Journal of Botany 96: 2010-2021 (2009) © 2009 Botanical Society of America, Inc. |
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Evolution and Phylogeny |
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, A316 Earth and Marine Sciences Building, Santa Cruz, California 95064 USA
ABSTRACT
Abiotically extreme environments are often associated with physiologically stressful conditions, small, low-density populations, and depauperate flora and fauna relative to more benign settings. A possible consequence of this may be that organisms that occupy these stressful habitats receive fitness benefits associated with reductions in the frequency and/or intensity of antagonistic species interactions. I investigated a particular form of this effect, formalized as the "pathogen refuge hypothesis," through a study of 13 species of wild flax that grow on stressful serpentine soils and are often infected by a pathogenic fungal rust. The host species vary in the degree of their serpentine association: some specialize on extreme serpentine soils, while others are generalists that occur on soils with a wide range of serpentine influence. Phylogenetically explicit analyses of soil chemistry and field-measured disease levels indicated that rust disease was significantly less frequent and severe in flax populations growing in more stressful, low-calcium serpentine soils. These findings may help to explain the persistence of extremophile species in habitats where stressful physical conditions often impose strong autecological fitness costs on associated organisms. Ancestral state reconstruction of serpentine soil tolerance (approximated using soil calcium concentrations) suggested that the ability to tolerate extreme serpentine soils may have evolved multiple times within the focal genus.
Key Words: edaphic specialization • Hesperolinon • Linaceae • Melampsora lini • pathogen refuge hypothesis • plant–pathogen interactions • serpentine soil • soil calcium • Uredinales
Received for publication 8 February 2009. Accepted for publication 2 July 2009.
FOOTNOTES
1 Many thanks to P. Aigner, K. Andonian, J. Callizo, S. Harrison, K. Koehler, H. Livingston, A. Lyman, N. McCarten, and J. Ruygt for help in the field and to numerous public and private landholders for access to their properties. R. Franks helped with edaphic testing, and assistance with genetic analyses was provided by M. Burford, K. Dlugosch, C. Fernandez, R. Kao, K. Kober, A. Koehler, K. Mesa, G. Pogson, M. Ramon, K. Rich, and J. Richardson. Comments and suggestions from B. Baldwin, M. Carr, A. Corl, G. Gilbert, T. Givnish, D. O’Donnell, M. Simmons, members of the ecoparasitology group at the University of Otago, and three anonymous reviewers greatly improved the analyses and writing of the manuscript. Financial support for this work was provided by the California Native Plant Society (state level and East Bay chapter), a Hardman Native Plant Research Fellowship, a generous donation from R. Poulin, and a grant from the UC Davis Genetic Resources Conservation Program. The genetic samples used in this study, as well as purified genomic DNA from three to six additional individuals from each study population and seeds from the majority of these populations, are available from the author.
2 Author for correrspondence: (e-mail: yurispringer{at}gmail.com)
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