Origin of a Complex Key Innovation in an Obligate Insect-Plant Mutualism Author(s): Olle Pellmyr and Harald W. Krenn Source: Proceedings of the National Academy of Sciences of the United States of America, Vol. 99, No. 8 (Apr. 16, 2002), pp. 5498-5502 Published by: National Academy of Sciences Stable URL: http://www.jstor.org/stable/3058521 Accessed: 24/01/2010 21:31 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=nas. 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Krenn* *Department of Biology, Vanderbilt University, Box 1812 Station B, Nashville, TN 37 235; and *Department of Evolutionary Biology, Institute of Zoology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria Edited by May R. Berenbaum, University of Illinois at Urbana-Champaign, Urbana, IL, and approved January 30, 2002 (received for review November 2, 2001) Evolutionary key innovations give organisms access to new eco- cle s to propose a possible developmental genetic basis for the logical resources and cause rapid, sometimes spectacular adaptive trait. radiation.The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of The Functionof the Tentacles.The pollinating yucca moth genera coevolution, and it relies on the key innovation in the moths of Te geticula and Parategeticula constitute a monophyletic group complex tentacles used for pollen collecting and active pollination. wi :hin the Prodoxidae (Fig. 1). Jointly they contain at least 25 These structures lack apparent homology in other insects, making ex :ant species (5), two of which are derived nonpollinating them a rareexample of a novel limb. We performed anatomical and Tegeticula species that oviposit into yucca fruit created by behavioral studies to determine their origin and found evidence of co existing pollinator species (16). The sister group Prodoxus a remarkably simple mechanism. Morphological analyses of the co exists with the pollinators on yuccas but feed as larvae on plant tentacles and adjacent mouthparts in pollinators and closely re- pa rts other than the seeds. Their radiation was thus directly lated taxa showed that the tentacle appears abruptly in female fa?:ilitated by the pollinator radiation. Together these genera pollinating yucca moths. Several morphological synapomorphies co nstitute a major adaptive radiation on yuccas, with a species between the galeae, which constitute the characteristic lepidop- di),ersity more than 20-fold that of their sister group, the teran proboscis, and the tentacle suggest that the tentacle evolved nc npollinating seed-parasitic Mesepiola, whose larvae feed on quicklythrough expression of the genetic template for the galea at ph ints in the Nolinaceae (17). an apical growth bud on the first segment of the maxillary palp. Female yucca moths possess unique tentacles on their mouth- Behavioral data indicate that tentacle and proboscis movements pa rts that are used to actively pollinate host flowers where they are controlled by a shared hydraulicextension mechanism, thus no ov iposit. The female moth gathers the glutinous pollen of yucca new mechanism was needed for tentacle function. Known devel- flc 'wers by scraping it off the anthers with her tentacles. The opmental paths from other insects can explain the origin of this po Ilen is immediately compacted by using tentacles and some- sex-specific key innovation in a few steps. tir les the forelegs as well, and placed as a solid batch on the co ncave posterioventral surface of the head (Fig. 2). The pollen iss and to 10% of the mutualisms between plants and pollinators provide m; may approach 10,000 grains weigh up O bligate )th mass Prolific maintains batch some of the most examples of coevolution (1, 2). ml body (18). pollen coating apparent co and the tentacles are not involved in its retention. A association of this kind, between yucca moths hesion, long-recognized ter the moth seeks out (Prodoxidae) and yucca plants (Agavaceae), has become an Ai pollen gathering, flowering yucca model in how mutualisms p1 ints where she oviposits into (Tegeticula) or near (Paratege- important understanding obligate As is the female flexes her coevolve In this association, established at least 40 million tic ula) pistils. oviposition completed, (3-6). itacles and uses the to remove a small are moths, te] apical portion pollen years ago (7), yuccas pollinated exclusively by yucca floral and whose larvae in turn consume some of the lo id from her batch. She walks to the stigma very developing yucca the on it. In all but one host seeds. This has been an and e liberately places pollen species, evolutionarily ecologically highly - line the interior of the hollow and the successful association, with some 30-45 stigmatic papillae style, yucca species (8, 9) )th in the with 10-20 motions much of the m' packs pollen repeated bobbing being important vegetation components throughout the course of 3-10 sec which is available as North American deserts and semiarid n (Movie 1, regions (10). information on the PNAS web In Prior of the coevolution between moths and su pporting site, www.pnas.org). analyses yucca - the host has a have shown that the transition from to single exception, (Hesperoyucca whipplei) yuccas antagonism ca and the moth the same mutualism involved in Cap-shaped stigma, pollinates by using primarily quantitative changes already behavior on the as is used for collection rather than novelties. The one agging stigma pollen existing traits, evolutionary the anthers. exception is the evolution of elaborate tentacular mouthparts in on the yucca moths, used for handling pollen with great precision. M rterials and Methods These tentacles are an evolutionary key innovation, both in the ale and female moths of six species were included in the study sense that it is a truly novel trait that evolved quickly (7) (Fig. 1) ig. 1). Two outgroup taxa were used to determine the basal and that it is linked to an adaptive radiation (11-13). Under- ( COndition. Nemophora degeerella(Adelidae) is a basal member of standing how this trait evolved, then, is central to understanding th superfamily Incurvarioidea, which includes Prodoxidae. the coevolutionary history of diversification and changing inter- p odoxus decipiens represents the pollinator sister group, thus actions between yuccas and yucca moths. Although reported be ing a close relative of the common ancestor of the tentacle- when the relationship was first described over a century ago (14, be aring moths of Tegeticula and Parategeticula. A clade of three 15), no analyses have been performed of tentacle anatomy or homology. Here we present anatomical data from phylogenetically piv- This paper was submitted directly(Track II) to the PNASoffice. otal moth species indicating that this complex key morphological tTcwhom reprintrequests should be addressed.E-mail: [email protected]. for the mutualism has a We also Th trait surprisingly simple origin. publicationcosts of this articlewere defrayed in part by page charge payment. This use trait expression in the pollinators, their nonpollinating sister artcle must therefore be hereby marked "advertisement"in accordancewith 18 U.S.C. group, and derived species that have secondarily lost the tenta- ?1;34 solely to indicatethis fact. 5498-5502 | PNAS | April16, 2002 | vol. 99 I no. 8 www.pnas.org/cgi/doi/10.1 073/pnas.072588699 CS3 : ( cr u, Pr czr X 7Tegeticula / tentacles lost .'. tentacles present (pollination) Prodoxidae Adelidae yuccas colonized Fig.1. Phylogeneticpositions of the sixspecies used in the study.Names of speciesused are given at top. Triangle width reflects species richness for the three yucca-feeding genera and their sister group. Spacing between prodoxid genera an i the Tegeticula species triad is proportional to time, and the bottoms of triangles give deepest known radiationswithin each genus. The deepest split (Mesepiola vs. others) is estimated to 44.1 + 10.6 millionyears ago. The internode from the Prodoxus-pollinatorgenera split to the pollinator genera split, along whic 1 the tentacle evolved, is so short that estimated ages of the three genera overlap, thus the uniform tentacle seen in all pollinator moths must have evolved veryquickly. Data are fromrefs. 5 and 7, and O.P.and M. Balcazar-Lara, unpublished data. Tegeticulaspecies was used, includingthe pollinatorsTegeticula pc llinating species of Tegeticula and Parategeticula (Fig. 3). yuccasellaand Tegeticulacassandra, and the derivednonpollina- M ales possess a small cuticle elevation in the same area (Fig. 3B). tor Tegeticulaintermedia. T. intermediarecently diverged from T. N() traces of a tentacle were found in either Prodoxus or cassandra (5), thus providing information on loss of the tenta- NMmophora.