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Plant Adaptation: Molecular Genetics and Ecology 12 3 4 1. Individuals of Mimulus guttatus (an outcrosser with large flowers) and M. alsinoides (a selfer with small flowers). See Chapter 3. Photo credit: Kermit Ritland. 2. Flowers of Piriqueta. See Chapter 9. Photo credit: Mitch Cruzan. 3. Lasthenia californica shown growing in a pasture in California. See Chapter 13. Photo credit: Nishanta Rajakaruna. 4. Variation in flower size in individuals of Collinsia parviflora grown under uniform conditions. See Chapter 14. Photo credit: Elizabeth Elle. Plant Adaptation: Molecular Genetics and Ecology Proceedings of an International Workshop sponsored by the UBC Botanical Garden and Centre for Plant Research held December 11–13, 2002 in Vancouver, British Columbia, Canada Edited by Q.C.B. Cronk, J. Whitton, R.H. Ree, and I.E.P. Taylor NRC Research Press Ottawa 2004 Q.C.B. Cronk, R.H. Ree1, and I.E.P. Taylor. UBC Botanical Garden and Centre for Plant Research, 6804 SW Marine Drive, Vancouver, BC V6T 1Z4, Canada. J. Whitton. Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada 1Current address: Field Museum, 1400 S. Lake Shore Dr, Chicago, IL 60605-2496, U.S.A. © 2004 National Research Council of Canada All rights reserved. No part of this publication may be reproduced in a retrieval system, or transmitted by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the National Research Council of Canada, Ottawa, Ontario K1A 0R6, Canada. Printed in Canada on acid-free paper. ISBN 0-660-19336-1 Electronic ISBN 0-660-19337-X NRC No. 46336 National Library of Canada cataloguing in publication Main entry under title: Plant adaptation: molecular genetics and ecology “Proceedings of an International Workshop sponsored by the UBC Botanical Garden and Centre for Plant Research held December 11–13, 2002 in Vancouver, British Columbia, Canada” Includes bibliographical references. Issued by the National Research Council of Canada. Issued also on the Internet. ISBN 0-660-19336-1 Cat. no. NR15-72/2002E 1. Plants — Adaptation — Congresses. 2. Plant ecological genetics — Congresses. 3. Plant genetics — Congresses. 4. Plant ecophysiology — Congresses. I. Cronk, Quentin C.B. II National Research Council Canada. QK912.M64 2004 581.4 C2004-980208-9 Inquiries: Proceedings Program, NRC Research Press, National Research Council of Canada, Ottawa, Ontario K1A 0R6, Canada. Cover illustration: The cover image was taken on Shell Island, British Columbia and shows a large population of sea blush, Plectritis congesta in the foreground. Most P. congesta populations are polymorphic for the presence or absence of wings on their fruits. Although the presence of wings is dominant, the polymorphism is hypothesized to be maintained by heterozygote advantage. It is not known whether pleiotropy or linkage contribute to fitness differences among genotypes. Photo credit: Peter Arcese Correct citation for this publication: Cronk, Q.C.B., Whitton, J., Ree, R.H., and Taylor, I.E.P. (Editors). 2004. Plant Adaptation: Molecular Genetics and Ecology. Proceedings of an International Workshop sponsored by the UBC Botanical Garden and Centre for Plant Research held December 11–13, 2002, in Vancouver, British Colum- bia, Canada. NRC Research Press, Ottawa, Ontario, Canada. 166 pp. v Contents Introduction: concepts in plant adaptation ...........................1 Chapter 1. The new science of adaptation: an introduction......................3 Quentin C.B. Cronk Chapter 2. Discussion report: an intellectual framework for a plant adaptation science ..........7 Richard Ree Chapter 3. Pathways to plant population genomics ........................11 Kermit Ritland Chapter 4. Evolvability and the raw materials for adaptation ....................18 Carl D. Schlichting and Courtney J. Murren Chapter 5. Nucleocytoplasmic incompatibility fosters speciation ...................30 Donald A. Levin Chapter 6. Discussion report: answered and unanswered questions in plant adaptation .........38 Brian C. Husband Approaches to the study of plant adaptation ..........................43 Chapter 7. Plant population genomics, linkage disequilibrium mapping and the genetics of adaptation. 45 Kenneth M. Olsen and Michael D. Purugganan Chapter 8. Genomic approaches to identifying quantitative trait loci: lessons from Arabidopsis thaliana ..53 Justin Borevitz Chapter 9. Experimental analysis of adaptive landscape topographies.................61 Mitchell B. Cruzan and Jennifer M. Rhode Chapter 10. Terpene synthases and the mediation of plant-insect ecological interactions byterpenoids:amini-review............................70 Dezene P.W. Huber and Jörg Bohlmann Chapter 11. Adaptation in plant speciation: empirical evidence for the role of selection in the evolution of isolating barriers between plant species................82 Leonie C. Moyle Chapter 12. Discussion report: new methods and tools for plant adaptation – what do we need? .....94 Barbara K. Mable Traits, populations, and species: case studies in plant adaptation ................101 Chapter 13. Trends in the evolution of edaphic specialists with an example of parallel evolution in the Lasthenia californica complex...........................103 Nishanta Rajakaruna and Jeannette Whitton Chapter 14. Floral adaptations and biotic and abiotic selection pressures...............111 Elizabeth Elle Chapter 15. Polyploidy and plant adaptation: a framework for future research ............119 Brian C. Husband Chapter 16. Evolutionary genetics of self-incompatibility in a new “model” plant: Arabidopsis lyrata . 127 Barbara K. Mable vi Chapter 17. Natural variation among accessions of Arabidopsis thaliana: beyond the flowering date, what morphological traits are relevant to study adaptation? ........135 X. Reboud, V. Le Corre, N. Scarcelli, F. Roux, J.L. David, T. Bataillon, C. Camilleri, D. Brunel, and H. McKhann Chapter 18. The study of ancient adaptation: a case study of a phytochrome gene pair from early-diverging angiosperms ..........................143 Sarah Mathews Chapter 19. The variable nature of herbivore defense: evidence for a rapidly diverging Kunitz trypsin inhibitor gene in Populus .......................153 Manoela Miranda, Mary Christopher, and C. Peter Constabel List of participants .....................................159 Index ...........................................161 INTRODUCTION: CONCEPTS IN PLANT ADAPTATION This page is intentionally blank 3 1 The new science of adaptation: an introduction Quentin C.B. Cronk The adaptive recursion much harder to study. This may be particularly true of plants. As plants are prone to phenotypic plasticity it is diffi- Adaptive recursion is a term borrowed from computer sci- cult to quantify the phenotype except in controlled growth ence. A recursive algorithm is a program that runs a new chambers. Phenotypic plasticity may also complicate the version of itself, by calling itself as it runs. Such recursion link from genotype to phenotype. Other problems include can be used, for instance, when searching down a directory the clonal reproduction of plants, which complicates the tree, or, in the case of adaptive algorithms, to optimize an scoring of allele frequencies. outcome (Smithies et al. 2004). There are obvious parallels between adaptive algorithms and biological adaptation. Adaptive recursion in computing involves a repeated pro- cess, the repeat being dependent upon on the preceding re- The Gould objection and neutrality as a null peat in a particular way. In biological adaptation the hypothesis “adaptive recursion” is the cycle from gene sequences to their unfolding as functional phenotypes that then interact A cursory look at the natural world provides hundreds of with the environment leading to gene frequency change in apparent instances of the fitting of form to function in natural populations, and so back to a different starting set of plants. However, the uncritical acceptance of ecological de- gene sequences. The programme then repeats in a manner terminism prior to the rejection of the appropriate null neu- that is dependent on the previous iteration. In computing it is tral hypothesis has led uncritically to the conclusion that important to avoid an infinite loop. In biology however the adaptive evolution is widespread. Naturalists after Darwin recursion is potentially infinite, only terminated on extinc- chronicled hundreds of instances of form following pre- tion. sumed function as evidence of adaptive evolution (Kerner In most cases the adaptive recursion is only studied by von Marilaun and Oliver 1902; Lubbock 1905; Fritsch and looking at single parts, such as molecular evolution or or- Salisbury 1953). One example is the prevalence of xero- ganism-environment interactions. One study that has been morphic leaves in dry habitats, apparently conferring resis- able to examine a substantial chunk of the adaptive recursion tance to water loss (see Table 1). However, physiological is that of Jamaican click beetles (Pyrophorus plagiophthala- tests of functional efficacy are rare (Givnish 2003; Givnish mus) and their evolving luminescence (Stolz et al. 2003). et al. 2004), and tests of selective advantage rarer still. Thus This is an ideal system for studying the adaptive recursion the idea that these “adaptations” are the result of adaptive for a number of reasons. First, the beetles are polymorphic evolution has remained speculation only in most cases. for an easily quantified