Origin of a complex key innovation in an obligateinsect–plant mutualismOlle Pellmyr*†and Harald W. Krenn‡*Department of Biology, Vanderbilt University, Box 1812 Station B, Nashville, TN 37235; and‡Department of Evolutionary Biology, Institute of Zoology,University of Vienna, Althanstrasse 14, A-1090 Vienna, AustriaEdited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved January 30, 2002 (received for reviewNovember 2, 2001)Evolutionary key innovations give organisms access to new eco-logical resources and cause rapid, sometimes spectacular adaptiveradiation. The well known obligate pollination mutualism betweenyuccas and yucca moths is a major model system for studies ofcoevolution, and it relies on the key innovation in the moths ofcomplex tentacles used for pollen collecting and active pollination.These structures lack apparent homology in other insects, makingthem a rare example of a novel limb. We performed anatomical andbehavioral studies to determine their origin and found evidence ofa remarkably simple mechanism. Morphological analyses of thetentacles and adjacent mouthparts in pollinators and closely re-lated taxa showed that the tentacle appears abruptly in femalepollinating yucca moths. Several morphological synapomorphiesbetween the galeae, which constitute the characteristic lepidop-teran proboscis, and the tentacle suggest that the tentacle evolvedquickly through expression of the genetic template for the galea atan apical growth bud on the first segment of the maxillary palp.Behavioral data indicate that tentacle and proboscis movementsare controlled by a shared hydraulic extension mechanism, thus nonew mechanism was needed for tentacle function. Known devel-opmental paths from other insects can explain the origin of thissex-specific key innovation in a few steps.Obligate mutualisms between plants and pollinators providesome of the most apparent examples of coevolution (1, 2).A long-recognized association of this kind, between yucca moths(Prodoxidae) and yucca plants (Agavaceae), has become animportant model in understanding how obligate mutualismscoevolve (3–6). In this association, established at least 40 millionyears ago (7), yuccas are pollinated exclusively by yucca moths,whose larvae in turn consume some of the developing yuccaseeds. This has been an evolutionarily and ecologically highlysuccessful association, with some 30–45 yucca species (8, 9)being important vegetation components throughout much of theNorth American deserts and semiarid regions (10).Prior analyses of the coevolution between yucca moths andyuccas have shown that the transition from antagonism tomutualism primarily involved quantitative changes in alreadyexisting traits, rather than evolutionary novelties. The oneexception is the evolution of elaborate tentacular mouthparts inthe yucca moths, used for handling pollen with great precision.These tentacles are an evolutionary key innovation, both in thesense that it is a truly novel trait that evolved quickly (7) (Fig. 1)and that it is linked to an adaptive radiation (11–13). Under-standing how this trait evolved, then, is central to understandingthe coevolutionary history of diversification and changing inter-actions between yuccas and yucca moths. Although reportedwhen the relationship was first described over a century ago (14,15), no analyses have been performed of tentacle anatomy orhomology.Here we present anatomical data from phylogenetically piv-otal moth species indicating that this complex key morphologicaltrait for the mutualism has a surprisingly simple origin. We alsouse trait expression in the pollinators, their nonpollinating sistergroup, and derived species that have secondarily lost the tenta-cles to propose a possible developmental genetic basis for thetrait.The Function of the Tentacles. The pollinating yucca moth generaTegeticula and Parategeticula constitute a monophyletic groupwithin the Prodoxidae (Fig. 1). Jointly they contain at least 25extant species (5), two of which are derived nonpollinatingTegeticula species that oviposit into yucca fruit created bycoexisting pollinator species (16). The sister group Prodoxuscoexists with the pollinators on yuccas but feed as larvae on plantparts other than the seeds. Their radiation was thus directlyfacilitated by the pollinator radiation. Together these generaconstitute a major adaptive radiation on yuccas, with a speciesdiversity more than 20-fold that of their sister group, thenonpollinating seed-parasitic Mesepiola, whose larvae feed onplants in the Nolinaceae (17).Female yucca moths possess unique tentacles on their mouth-parts that are used to actively pollinate host flowers where theyoviposit. The female moth gathers the glutinous pollen of yuccaflowers by scraping it off the anthers with her tentacles. Thepollen is immediately compacted by using tentacles and some-times the forelegs as well, and placed as a solid batch on theconcave posterioventral surface of the head (Fig. 2). The pollenmass may approach 10,000 grains and weigh up to 10% of themoth body mass (18). Prolific pollen coating maintains batchcohesion, and the tentacles are not involved in its retention.After pollen gathering, the moth seeks out flowering yuccaplants where she oviposits into (Tegeticula) or near (Paratege-ticula) pistils. As oviposition is completed, the female flexes hertentacles and uses the apical portion to remove a small pollenload from her batch. She walks to the floral stigma and verydeliberately places the pollen on it. In all but one host species,the stigmatic papillae line the interior of the hollow style, and themoth packs in the pollen with 10–20 repeated bobbing motionsin the course of 3–10 sec (Movie 1, which is available assupporting information on the PNAS web site, www.pnas.org). Inthe single exception, the host (Hesperoyucca whipplei) has acap-shaped stigma, and the moth pollinates by using the samedragging behavior on the stigma as is used for pollen collectionon the anthers.Materials and MethodsMale and female moths of six species were included in the study(Fig. 1). Two outgroup taxa were used to determine the basalcondition. Nemophora degeerella (Adelidae) is a basal member ofthe superfamily Incurvarioidea, which includes Prodoxidae.Prodoxus decipiens represents the pollinator sister group, thusbeing a close relative of the common ancestor of the tentacle-bearing moths of Tegeticula and Parategeticula. A clade of
View Full Document
Unlocking...