Origin of a complex key innovation in an obligate insect plant mutualism Olle 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 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 ecological resources and cause rapid sometimes spectacular adaptive radiation The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of coevolution and it relies on the key innovation in the moths of complex tentacles used for pollen collecting and active pollination These structures lack apparent homology in other insects making them a rare example of a novel limb We performed anatomical and behavioral studies to determine their origin and found evidence of a remarkably simple mechanism Morphological analyses of the tentacles and adjacent mouthparts in pollinators and closely related taxa showed that the tentacle appears abruptly in female pollinating yucca moths Several morphological synapomorphies between the galeae which constitute the characteristic lepidopteran proboscis and the tentacle suggest that the tentacle evolved quickly through expression of the genetic template for the galea at an apical growth bud on the first segment of the maxillary palp Behavioral data indicate that tentacle and proboscis movements are controlled by a shared hydraulic extension mechanism thus no new mechanism was needed for tentacle function Known developmental paths from other insects can explain the origin of this sex specific key innovation in a few steps O bligate mutualisms between plants and pollinators provide some 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 an important model in understanding how obligate mutualisms coevolve 3 6 In this association established at least 40 million years ago 7 yuccas are pollinated exclusively by yucca moths whose larvae in turn consume some of the developing yucca seeds This has been an evolutionarily and ecologically highly successful association with some 30 45 yucca species 8 9 being important vegetation components throughout much of the North American deserts and semiarid regions 10 Prior analyses of the coevolution between yucca moths and yuccas have shown that the transition from antagonism to mutualism primarily involved quantitative changes in already existing traits rather than evolutionary novelties The one exception is the evolution of elaborate tentacular mouthparts in the yucca moths used for handling pollen with great precision These tentacles are an evolutionary key innovation both in the sense that it is a truly novel trait that evolved quickly 7 Fig 1 and that it is linked to an adaptive radiation 11 13 Understanding how this trait evolved then is central to understanding the coevolutionary history of diversification and changing interactions between yuccas and yucca moths Although reported when the relationship was first described over a century ago 14 15 no analyses have been performed of tentacle anatomy or homology Here we present anatomical data from phylogenetically pivotal moth species indicating that this complex key morphological trait for the mutualism has a surprisingly simple origin We also use trait expression in the pollinators their nonpollinating sister group and derived species that have secondarily lost the tenta5498 5502 PNAS April 16 2002 vol 99 no 8 cles to propose a possible developmental genetic basis for the trait The Function of the Tentacles The pollinating yucca moth genera Tegeticula and Parategeticula constitute a monophyletic group within the Prodoxidae Fig 1 Jointly they contain at least 25 extant species 5 two of which are derived nonpollinating Tegeticula species that oviposit into yucca fruit created by coexisting pollinator species 16 The sister group Prodoxus coexists with the pollinators on yuccas but feed as larvae on plant parts other than the seeds Their radiation was thus directly facilitated by the pollinator radiation Together these genera constitute a major adaptive radiation on yuccas with a species diversity more than 20 fold that of their sister group the nonpollinating seed parasitic Mesepiola whose larvae feed on plants in the Nolinaceae 17 Female yucca moths possess unique tentacles on their mouthparts that are used to actively pollinate host flowers where they oviposit The female moth gathers the glutinous pollen of yucca flowers by scraping it off the anthers with her tentacles The pollen is immediately compacted by using tentacles and sometimes the forelegs as well and placed as a solid batch on the concave posterioventral surface of the head Fig 2 The pollen mass may approach 10 000 grains and weigh up to 10 of the moth body mass 18 Prolific pollen coating maintains batch cohesion and the tentacles are not involved in its retention After pollen gathering the moth seeks out flowering yucca plants where she oviposits into Tegeticula or near Parategeticula pistils As oviposition is completed the female flexes her tentacles and uses the apical portion to remove a small pollen load from her batch She walks to the floral stigma and very deliberately places the pollen on it In all but one host species the stigmatic papillae line the interior of the hollow style and the moth packs in the pollen with 10 20 repeated bobbing motions in the course of 3 10 sec Movie 1 which is available as supporting information on the PNAS web site www pnas org In the single exception the host Hesperoyucca whipplei has a cap shaped stigma and the moth pollinates by using the same dragging behavior on the stigma as is used for pollen collection on the anthers Materials and Methods Male and female moths of six species were included in the study Fig 1 Two outgroup taxa were used to determine the basal condition Nemophora degeerella Adelidae is a basal member of the superfamily Incurvarioidea which includes Prodoxidae Prodoxus decipiens represents the pollinator sister group thus being a close relative of the common ancestor of the tentaclebearing moths of Tegeticula and Parategeticula A clade of three This paper was submitted directly Track
View Full Document
Unlocking...