Chemical and Mechanical Defenses Vary among Maternal Lines and Leaf Ages in Verbascum thapsus L. (Scrophulariaceae) and Reduce Palatability to a Generalist Insect

Chemical and Mechanical Defenses Vary among Maternal Lines and Leaf Ages in Verbascum thapsus L. (Scrophulariaceae) and Reduce Palatability to a Generalist Insect Christina Alba 0 M. Deane Bowers 0 Dana Blumenthal 0 Ruth A. Hufbauer 0 0 1 Graduate Degree Program in Ecology and Department of Bioagricultural Sciences and Pest Management, Colorado State University , Fort Collins , Colorado, United States of America, 2 University of Colorado at Boulder, Department of Ecology and Evolutionary Biology, Boulder, Colorado, United States of America , 3 USDA-ARS, Fort Collins, Colorado , United States of America Intra-specific variation in host-plant quality affects herbivore foraging decisions and, in turn, herbivore foraging decisions mediate plant fitness. In particular, variation in defenses against herbivores, both among and within plants, shapes herbivore behavior. If variation in defenses is genetically based, it can respond to natural selection by herbivores. We quantified intra-specific variation in iridoid glycosides, trichome length, and leaf strength in common mullein (Verbascum thapsus L, Scrophulariaceae) among maternal lines within a population and among leaves within plants, and related this variation to feeding preferences of a generalist herbivore, Trichopulsia ni H ubner. We found significant variation in all three defenses among maternal lines, with T. ni preferring plants with lower investment in chemical, but not mechanical, defense. Within plants, old leaves had lower levels of all defenses than young leaves, and were strongly preferred by T. ni. Caterpillars also preferred leaves with trichomes removed to leaves with trichomes intact. Differences among maternal lines indicate that phenotypic variation in defenses likely has a genetic basis. Furthermore, these results reveal that the feeding behaviors of T. ni map onto variation in plant defense in a predictable way. This work highlights the importance of variation in hostplant quality in driving interactions between plants and their herbivores. - Citation: Alba C, Bowers MD, Blumenthal D, Hufbauer RA (2014) Chemical and Mechanical Defenses Vary among Maternal Lines and Leaf Ages in Verbascum thapsus L. (Scrophulariaceae) and Reduce Palatability to a Generalist Insect. PLoS ONE 9(8): e104889. doi:10.1371/journal.pone.0104889 Editor: Benedicte Riber Albrectsen, Umea Plant Science Centre, Umea University, Sweden Received March 21, 2014; Accepted July 16, 2014; Published August 15, 2014 This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files. Funding: RH was supported by the United States Department of Agriculture, Colorado Agricultural Experiment Station (grant numbers COL00680 and COL00222A; URL aes.agsci.colostate.edu). CA received support from the Harold David Harrington Graduate Fellowship administered through the Biology Department at Colorado State University. Funding for page charges was provided by the Colorado State University Libraries Open Access Research and Scholarship Fund. CA was funded by long-term research development project no. RVO 67985939 from the Academy of Sciences of the Czech Republic (URL http://cas.cz) during the writing of this paper. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: Current address: Institute of Botany, Academy of Sciences of the Czech Republic, Pruhonice, Czech Republic Host-plant quality, which is the balance between nutrients and defenses in plant tissues that influences herbivores [1], varies within as well as between species. Intra-specific variation in hostplant quality can shape herbivore community dynamics by influencing herbivore abundance and distribution [2], [3], for example when herbivores preferentially feed on different plant genotypes within a population [2]. Further, because differences in nutritional value and levels of defense among individual plants or plant tissues affect patterns of herbivory, they may feed back to determine plant fitness [4]. Intra-specific variation in plant quality also influences higher trophic levels, due to both differences in herbivore abundance and differences in the quality of herbivores as prey or hosts [5], [6]. Thus, characterizing intra-specific variation in host-plant quality, which is often manifested among maternal lines within a population, lies at the foundation of understanding plant-herbivore and herbivore-enemy interactions. Defenses against herbivores are a main determinant of hostplant quality [1], [7], and thus are particularly important to characterize. Heterogeneity in plant defense arises from variation in the particular type of chemical or mechanical defense a plant employs, and from variation in the amount of a given defense expressed in a plant or plant tissue. Chemical and mechanical defenses are hypothesized to differ in their effectiveness against herbivores with different diet breadths. In particular, while many chemical defenses tend to confer resistance against generalist herbivores via their deterrent or toxic effects [8], mechanical defenses, which present a physical barrier, typically confer resistance against both generalists and specialists [9]. The extent to which plants invest in chemical versus mechanical defense depends on many factors including resource availability, herbivore community composition, phylogenetic constraints, and whether defenses have non-redundant functions [10], [11], [12], [13], [14]. While there is evidence that resource-limited plants exhibit tradeoffs in investment among chemical and mechanical defenses [15], [16], a recent global survey of more than 260 plant species found that plants often invest highly in both, with little indication of trade-offs [17], [18]. This pattern suggests that natural selection favors the maintenance of an array of defenses with different efficacy against co-existing herbivore guilds [17]. Variation in defense occurs both among and within plants. Among individual plants, variation in maternal lines typically has a genetic basis (though environmentally driven maternal effects can also contribute) [19]. Maternal variation in defenses can be quite pronounced [20], [21], [22], with more highly defended maternal lines experiencing reduced oviposition and feeding damage [21], [22], [23] and higher fitness in the presence of herbivores [13]. Within plants, variation in levels of defenses among different tissues is common [24] [25]. In particular, che (...truncated)