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Phylogenetic and Experimental Tests of Interactions Among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae)

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Phylogenetic and Experimental Tests of Interactions Among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae) The University of Chicago Phylogenetic and Experimental Tests of Interactions among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae). Author(s): Marjorie G. Weber, Wendy L. Clement, Michael J. Donoghue, and Anurag A. Agrawal Reviewed work(s): Source: The American Naturalist, Vol. 180, No. 4 (October 2012), pp. 450-463 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/667584 . Accessed: 03/10/2012 13:30 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org vol. 180, no. 4 the american naturalist october 2012 Phylogenetic and Experimental Tests of Interactions among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae) Marjorie G. Weber,1,* Wendy L. Clement,2 Michael J. Donoghue,2 and Anurag A. Agrawal1 1. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853; 2. Department of Ecology and Evolutionary Biology, Yale University, P.O. Box 208105, New Haven, Connecticut 06520 Submitted October 7, 2011; Accepted May 30, 2012; Electronically published August 22, 2012 Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.t4n0g. which are plant organs that secrete sugary nectar and typ- abstract: Plant traits that mediate mutualistic interactions are ically feed beneficial arthropods (Bentley 1977; Heil 2008); widespread, yet few studies have linked their macroevolutionary pat- terns with the ecological interactions they mediate. Here we merged and (2) leaf domatia, which are small structures on the phylogenetic and experimental approaches to investigate the evolu- undersides of leaves that provide housing for predaceous tion of two common mutualistic plant traits, extrafloral nectaries or fungivorous mites (Lundstro¨m 1887; Romero and Ben- (EFNs) and leaf domatia. By using the flowering plant clade Vibur- son 2005). Because traits such as EFNs and leaf domatia num, we tested whether macroevolutionary patterns support adaptive influence multiple trophic levels, their evolution can have hypotheses and conducted field surveys and manipulative experi- ments to examine whether ecological interactions are concordant strong impacts on community dynamics relative to other with evolutionary predictions. Phylogenetic reconstructions sug- plant characters. Nonetheless, studies that directly link pat- gested that EFN-bearing species are monophyletic, whereas the evo- terns in the evolution of these traits to their contemporary lution of domatia correlated with leaf production strategy (deciduous ecological function are rare (but see Karban et al. 1995; or evergreen) and climate. Domatia were also more common in the Heil et al. 2004). EFN clade, suggesting that the two traits may jointly mediate eco- Several hypotheses attempt to explain the evolution and logical interactions. This result was further investigated in a com- mon-garden survey, where plants with domatia and EFNs on the leaf phylogenetic distribution of mutualistic defense traits such blade had more mutualistic mites than plants with other trait com- as EFNs and leaf domatia. These hypotheses are primarily binations, and in manipulative field experiments, where the traits focused on two factors: (1) the adaptive value of mutu- additively increased mutualist abundance. Taken together, our results alistic defense traits in certain biotic or abiotic environ- suggest that mutualistic traits in Viburnum are not ecologically in- ments (e.g., Bentley 1977; Schupp and Feener 1991; Heil dependent, as they work in concert to attract and retain mutualists, and McKey 2003; Bronstein et al. 2006) and (2) evolu- and their long-term evolution may be influenced by complex inter- actions among multiple traits, mutualists, and geography. tionary trade-offs or synergisms with other ecologically relevant plant traits (e.g., Heil 2004, 2008). Environmental Keywords: bed-and-breakfast hypothesis, mite, mutualism, indirect hypotheses posit that large-scale geographic associations defense, Viburnum, extrafloral nectaries, leaf domatia. between mutualistic defense traits and environmental fac- tors are adaptive. For example, the well-established pattern Introduction of increased EFN prevalence in the tropics is hypothesized to be driven by selective forces that are both biotic (e.g., Despite being widespread and ecologically important, increased abundance, species richness, and aggressiveness plant traits that mediate mutualistic interactions are rarely of mutualists) and abiotic (e.g., higher resource availability studied in an integrative manner that spans phylogenetic and longer growing seasons; Bentley 1977; Schupp and and ecological scales (Bronstein et al. 2006). In plant- Feener 1991; Heil and McKey 2003; Bronstein et al. 2006). arthropod defense mutualisms, specialized plants traits Not all defense mutualisms are more prevalent in the trop- provide food or shelter rewards to arthropods in return ics, however: leaf tuft domatia are more frequently found for protection against natural enemies. Two well-known in temperate plant species, a pattern hypothesized to be examples of such traits are (1) extrafloral nectaries (EFNs), driven by increased risk of mite desiccation in temperate * Corresponding author; e-mail: [email protected]. climates (Romero and Benson 2005). A second set of hypotheses focuses on evolutionary Am. Nat. 2012. Vol. 180, pp. 450–463. ᭧ 2012 by The University of Chicago. 0003-0147/2012/18004-53380$15.00. All rights reserved. trade-offs or synergisms and suggests that the origin, main- DOI: 10.1086/667584 tenance, and breakdown of indirect defensive traits are Evolution of Indirect Defense Traits 451 influenced by interactions with other plant traits rather When historical patterns of macroevolution are con- than environmental factors alone. For example, indirect cordant with contemporary ecological dynamics, hypoth- defenses are hypothesized to positively associate with leaf eses that link pattern with process are more strongly sup- longevity (Bronstein et al. 2006) because plants with short- ported (Losos 1996, 2009; Weber and Agrawal 2012). lived leaves are predicted to invest less in defenses than Alternatively, the lack of concordance suggests that either those with longer-lived leaves (Coley 1988). Another hy- conditions have changed substantially over time or hy- pothesis suggests that multiple indirect defensive traits in- potheses need to be further refined (Losos 1996, 2009). teract with one another in a way that influences their In this study, we integrate comparative phylogenetics with ecological functions and, ultimately, their evolution (Heil field surveys and manipulative experiments to examine the 2008). For example, if two defensive traits are consistently combined evolution of mutualistic defense traits in Vi- ecologically redundant and costly, they are predicted to be burnum, a widespread clade of shrubs and small trees. negatively correlated across a phylogeny (Agrawal et al. Specifically, we ask the following questions: (1) Are pat- 2010). Alternatively, if traits exhibit additive or synergistic terns of mutualistic trait evolution consistent with existing ecological effects that are sustained over time, they may adaptive and trade-off or synergism hypotheses? In par- show positive correlated evolution. Heil and McKey (2003) ticular, do traits show correlated evolution with one an- suggested that mutualistic interactions are stronger and other, with other relevant plant traits, or with environ- more likely to be maintained over time when several traits ments hypothesized to influence their evolution? And (2) are found together, because mutualists are provided with do field surveys and manipulative experiments of the two multiple rewards (e.g., food and housing). Similarly, Fiala traits demonstrate ecological interactions that are consis- and Maschwitz (1992) suggested that ant domatia, in ad- tent with our interpretations of trait evolution patterns? dition to food-based rewards, are an important component in the evolution of obligate defense mutualisms in Mac- Methods aranga. In another example using Viburnum tinus, EFNs (Walter and O’Dowd 1995) and leaf domatia (Grostal and Viburnum (Adoxaceae, Dipsacales) is a clade of ∼170 spe- O’Dowd 1994) were each separately shown to increase the cies of understory shrubs and small trees. Viburnum nat- abundance of mutualistic mites living on leaves. Indeed, urally occurs in temperate forests around the Northern many striking defense mutualisms occur on plants that Hemisphere, with extensions into the Southern Hemi- reward their mutualists with several distinct beneficial sphere in tropical forests of Southeast Asia and cloud for- traits (Heil 2008), and yet their joint evolution has been ests of South America. Its two modern centers of species little studied. In particular, no study has examined the diversity are in Eastern Asia and Latin
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