Do Biochemical Exaptations Link Evolution of Defense and Pollination Systems? Historical Hypotheses and Experimental Tests with Dalechampia Vines

University of New Orleans ScholarWorks@UNO Biological Sciences Faculty Publications Department of Biological Sciences 3-1997 Do Biochemical Exaptations Link Evolution of Defense and Pollination Systems? Historical Hypotheses and Experimental Tests with Dalechampia Vines Jerome J. Howard University of New Orleans, [email protected] Follow this and additional works at: https://scholarworks.uno.edu/biosciences_facpubs Part of the Biology Commons Recommended Citation Armbruster, W.S., J.J. Howard, T.P. Clausen, E. Debevec, J. Loquvam, M. Matsuki, B. Cerendolo, and F. Andel. 1997. Do biochemical exaptations link evolution of defense and pollination systems? Historical hypotheses and experimental tests with Dalechampia vines. American Naturalist 149 (3): 461-484. This Article is brought to you for free and open access by the Department of Biological Sciences at ScholarWorks@UNO. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of ScholarWorks@UNO. For more information, please contact [email protected]. The University of Chicago Do Biochemical Exaptations Link Evolution of Plant Defense and Pollination Systems? Historical Hypotheses and Experimental Tests with Dalechampia Vines Author(s): W. Scott Armbruster, Jerome J. Howard, Thomas P. Clausen, Edward M. Debevec, John C. Loquvam, Mamoru Matsuki, Bianca Cerendolo and Frank Andel Reviewed work(s): Source: The American Naturalist, Vol. 149, No. 3 (Mar., 1997), pp. 461-484 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/2463378 . Accessed: 08/08/2012 12:07 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. 149,No. 3 The AmericanNaturalist March1997 DO BIOCHEMICAL EXAPTATIONS LINK EVOLUTION OF PLANT DEFENSE AND POLLINATION SYSTEMS? HISTORICAL HYPOTHESES AND EXPERIMENTAL TESTS WITH DALECHAMPIA VINES W. SCOTT ARMBRUSTER,"*JEROME J. HOWARD,1'tTHOMAS P. CLAUSEN,2EDWARD M. DEBEVEC,1 JOHNC. LOQUVAM,1MAMORU MATSUKI,1't BIANCA CERENDOLO,2 AND FRANKANDEL2 'Instituteof ArcticBiology and 2Departmentof Chemistry,University of Alaska, Fairbanks,Alaska 99775-7000 SubmittedOctober 16, 1995;Revised May 30, 1996;Accepted June 4, 1996 Abstract.-Mappingresin secretion and pollinationecology onto the estimated phylogeny of speciesof theeuphorb vine Dalechampia generated two historicalhypotheses: resin rewards offeredto pollinatorsby Dalechampia flowers evolved by minormodification of a preexisting, resin-based,floral defense system, and resindefense of leaves in advancedspecies evolved by modificationof thepreexisting resin-reward system. From these hypotheses, we derivedtwo predictions:floral reward resins are chemicallysimilar to putativefloral defense resins and exhibitantiherbivore activities, and foliarresins are chemicallysimilar to rewardresins and also exhibitantiherbivore activities. We testedthese predictions by chemicalanalyses and by usinga broadsample of Neotropical herbivorous insects in a seriesof bioassays. All floraland foliarresins were chemically similar. Tests with two generalist (Orophus tesselatus, Orthoptera: Tettigoniidae;Atta colombica, Hymenoptera: Formicidae) and four Dalechampia-specialist herbivores(Syphraea sp., Coleoptera:Chrysomelidae; Ectima rectifasciata, Hamadryas ipthime, andHamadryas amphinome, Lepidoptera: Nymphalidae) showed floral and foliar resin to deter significantlyfeeding or leaf cutting.These resultssupport our two hypothesesand indicate that,in thissystem, biochemical exaptations have playeda majorrole in the evolutionof plant-insectrelationships, adaptations reducing herbivory have affected the evolution of plant- pollinatorrelationships, and adaptationsfor pollination have affectedthe evolutionof plant- herbivorerelationships. Mutualismsand antagonismsbetween plants and animalsplay majorroles in the functionof biologicalcommunities (Gilbert and Raven 1975;Gilbert 1980; Thompson1982; Futuyma and Slatkin1983; Strong et al. 1984;Boucher 1985). Whilethe short-term ecological dynamics of plant-animal interactions have been reasonablywell studiedin a numberof systems,we knowrelatively little about how theserelationships originate and evolve (Thompson1982, 1994; Futuyma 1983;Schemske 1983; Boucher 1985; Mitter et al. 1988;Farrell et al. 1992;Farrell * To whomcorrespondence should be addressed;E-mail: [email protected]. t Presentaddress: Department of BiologicalSciences, University of New Orleans,New Orleans, Louisiana70148. t Presentaddress: Research School of BiologicalSciences, Australian National University, Can- berraACT 2601,Australia. Am. Nat. 1997. Vol. 149, pp. 461-484. ? 1997 by The Universityof Chicago. 0003-0147/97/4903-0003$02.00.All rightsreserved. 462 THE AMERICANNATURALIST and Mitter1994). For example,how do completelynew mutualistic or antagonis- ticinteractions come into existence? What constrains the evolution of interactions amongspecies? Do evolutionaryresponses of a populationto one set of inter- actingorganisms (e.g., herbivores)affect interactions with other organisms (e.g., pollinators)? Integrationof modernphylogenetic methods with ecological data is allowing these questionsto be addressedfrom a long-termevolutionary perspective, throughthe generationof explicithistorical hypotheses (see Mitteret al. 1988; Brooksand McLennan1991; Harvey and Pagel 1991;Armbruster 1992; Farrell et al. 1992; Farrelland Mitter1994; Thompson 1994). However, the historical hypotheseshave onlyrarely been testedwith independent data or experiments (see Armbruster1993; Pellmyr and Huth 1994; Pellmyr et al. 1996).In thepresent study,we synthesizedphylogenetic and ecological information to generate historical hypothesesabout the evolutionary relationship between plant pollination and antiherbivoredefense systems. We thendevised several ecological experiments to testthese hypotheses. EVOLUTION OF PLANT-ANIMAL RELATIONSHIPS The interactionsbetween plants and otherorganisms are commonlymediated by plantsecondary chemistry. Two featuresindicate that chemically mediated interactionsmay evolve rapidly. First, organisms often have highlyspecific re- sponsesto compounds,and minorstructural changes in a compoundmay result in majorchanges in biologicalactivity (e.g., Dodson et al. 1969;Farentinos et al. 1981;Reichardt et al. 1984;Bryant et al. 1992).Second, a singleplant compound mayaffect more than one interactingspecies (e.g., Clausenet al. 1986;Pellmyr and Thien1986; Bryant et al. 1991),and theevolution of plant secondary chemis- trymay be influencedby simultaneousinteractions with different functional groupsof organisms(e.g., pathogensvs. herbivoresvs. mutualists). Whilethe role of secondarycompounds in plantdefense (see reviewin Rosen- thaland Berenbaum 1992) might appear unrelated to a rolein attracting mutualists (see reviewin Simpsonand Neff1981), chemical similarities indicate that these tworoles may sometimes be linked.For example,1, 8-cineole,a monoterpene, is a strongdeterrent to snowshoehares and apparentlyfunctions as a defense compoundin balsampoplars (Populus balsamifera) in Alaska (Mattes et al. 1987; Reichardtet al. 1990).The same compoundis secretedby tropicalorchids and servesas an attractantand rewardto pollinatingmale-euglossine bees (Dodson et al. 1969).Thus, the possibilityexists that a singlecompound or mixtureof compoundsin a plantcould simultaneously, or sequentially(in developmentalor evolutionarytime), play several very different ecological roles. Pellmyr and Thien (1986) pointedout thatmany fragrances that attract pollinators to flowersare biochemicallysimilar to compoundsthat deter herbivores, and the same or similar compoundsmay play the role of attractionin theflowers and deterrencein the leaves. If thisis common,relatively small genetic changes could cause rapid shiftsin ecologicalrelationships between plants and theirmutualists and antagonists.This raises some interestingquestions. Do complexplant-animal interac- EVOLUTION OF PLANT DEFENSE AND REWARD SYSTEMS 463 tionsnecessarily reflect a longhistory of coevolution, as has oftenbeen thought? Or are ecologicalrelationships between plants and animalsoften evolutionarily labile,changing rapidly in responseto subtleselective pressures or stochastic events(see Pellmyrand Thompson1992)? Are biochemicalexaptations (sensu Gouldand Vrba 1982;i.e., preadaptations)important, and can newrelationships evolve suddenlyin species withpreaptations in place? Do plantrelationships withherbivores influence the evolution of plant-pollinatorinteractions and vice versa? EVOLUTION OF EUPHORB VINES To beginaddressing these questions, we investigatedthe chemical ecology of a modelplant-animal system: species of the tropicalplant genus Dalechampia (Euphorbiaceae)and their mutualists and antagonists. Most species of Dalecham- pia offeran unusualreward to pollinators:terpenoid resins. The resinis secreted byblossom

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