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Evolution of Gall Morphology and Host-Plant Relationships in Willow-Feeding Sawflies (Hymenoptera: Tenthredinidae)

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Evolution of Gall Morphology and Host-Plant Relationships in Willow-Feeding Sawflies (Hymenoptera: Tenthredinidae) Evolution, 54(2), 2000, pp. 526±533 EVOLUTION OF GALL MORPHOLOGY AND HOST-PLANT RELATIONSHIPS IN WILLOW-FEEDING SAWFLIES (HYMENOPTERA: TENTHREDINIDAE) TOMMI NYMAN,1,2 ALEX WIDMER,3 AND HEIKKI ROININEN1 1Department of Biology, University of Joensuu, P.O. Box 111, FIN-80101 Joensuu, Finland 2E-mail: tommi.nyman@joensuu.® 3Geobotanical Institute, ETH ZuÈrich, Zollikerstrasse 107, CH-8008 ZuÈrich, Switzerland Abstract. There are over 200 species of nematine saw¯ies that induce galls on willows (Salix spp.). Most of the species are mono- or oligophagous, and they can be separated into seven or eight different groups based on the type of gall that they induce. We studied the evolution of different gall types and host plant associations by reconstructing the phylogeny of ®ve outgroup and 31 ingroup species using DNA sequence data from the mitochondrial cytochrome b gene. Maximum-parsimony and maximum-likelihood analyses resulted in essentially the same phylogeny with high support for important branches. The results show that: (1) the galling species probably form a monophyletic group; (2) true closed galls evolved only once, via leaf folders; (3) with the possible exception of leaf rollers, all gall type groups are mono- or paraphyletic; (4) similar gall types are closer on the phylogeny than would be expected by a random process; (5) there is an apparent evolutionary trend in galling site from the leaf edge towards the more central parts of the host plant; and (6) many willow species have been colonized several times, which excludes the possiblity of parallel cladogenesis between willows and the gallers; however, there are signs of restrictions in the evolution of host use. Many of the patterns in the evolutionary history of nematine gallers have also been observed in earlier studies on other insect gallers, indicating convergent evolution between the independent radiations. Key words. Coevolution, convergent evolution, evolutionary trends, extended phenotypes, gall morphology, gradu- alism, insect-plant relationships, Nematinae, phylogeny. Received June 1, 1999. Accepted October 11, 1999. The habit of galling has evolved many times independently eight different gall types can be recognized. Thus, the struc- in various organisms (Meyer 1987). In insects alone, gall tural diversity of nematine galls rivals that of the cynipid induction has evolved in at least seven different orders, and wasp galls; however, the internal structure of the galls has in most of them several radiations have arisen (Meyer 1987; remained relatively uniform and simple. Each gall type can Dreger-Jauffret and Shorthouse 1992). The multiple origins be found on several species of willow, and several types of of galling makes it possible to search for convergent features gallers can coexist on each willow species (Kontuniemi 1960; in these independent evolutionary histories. Indeed, recent Roininen 1991). phylogenetic analyses of gall-inducing aphids (Stern 1995), Price (1992; see also Smith 1970; Roininen 1991) sug- wasps (Stone and Cook 1998), and thrips (Crespi and Wo- gested that the different gall types evolved gradually, that is, robey 1998) have shown that common features exist in sep- the evolutionary sequence would have been: (1) leaf folders/ arate radiations. For example, in all these taxa gall mor- rollers; (2) leaf blade gallers; (3) apical leaf gallers; (4) basal phology is determined mainly by the galler, not the host plant, leaf gallers; (5) petiole gallers; (6) stem gallers; and (7) bud and thus the gall can be considered an extended phenotype gallers. Thus, there would have been a slow, gradual process (sensu Dawkins 1982) of the galler. with radiations to new willow species after the evolution of The nematine saw¯ies that induce galls on willows (Salix each new gall type. In addition, there would have been an spp.) also offer a good model system for the study of evo- evolutionary trend toward earlier oviposition in the more cen- lutionary questions, especially questions about the evolution tral parts of the host plants and a more intimate relationship of different gall types and host plant associations (Price between galler and host (Price and Roininen 1993). 1992). These saw¯ies belong to the tenthredinid subfamily The gradualistic view is indeed tempting: In all species the Nematinae, which is comprised of hundreds of galling and galls are initiated by substances secreted by the ovipositing nongalling species (Smith 1979; Gauld and Bolton 1988). female into the oviposition scar (Price and Roininen 1993), There are about 200 species of galling nematines, most of and exact positioning of the egg is necessary for the gall to which are mono- or oligophagous (Smith 1970; Price et al. develop normally (McCalla et al. 1962). A change in gall 1994). Like their host plants, these saw¯ies are common and type would probably require simultaneous changes in ovi- have a mainly holarctic distribution (Smith 1979; Gauld and positor morphology and the oviposition behavior of females. Bolton 1988). Thus, small changes in the site of gall induction may be The nematine gallers have traditionally been treated as a considered to be more likely than large changes. separate tribe within the Nematinae, the Euurina (Vikberg In a previous paper (Nyman et al. 1998), we used enzyme 1982; Viitasaari and Vikberg 1985). The species have been electrophoretic data to test the Price-Roininen hypothesis. We divided into three genera, mainly on the basis of the type of were able to show that there are signs of constraints on the gall that they induce: Phyllocolpa species form leaf folds or evolution of gall types, and that gall type changes may be rolls; Pontania species are leaf blade gallers or apical/basal gradual. However, the limited taxonomic sample (18 species) leaf gallers; and Euura species induce petiole, stem, or bud and the low support for many of the groupings in the resulting galls (Meyer 1987; Price and Roininen 1993). In all, about phylogeny prevented us from reaching de®nite conclusions. 526 q 2000 The Society for the Study of Evolution. All rights reserved. SAWFLIES, GALLS, AND WILLOWS 527 TABLE 1. Species used in the study, their host plants, and sample sites. Gall type1 Species Willow host2 Sample site3/date 0. Outgroup Tenthredo arcuata (FoÈrster) Ð Joensuu (F), 1996 Nematus salicis (Linnaeus) Salix fragilis (S) Joensuu (F), 1996 Nematus capreae (Linnaeus) S. myrsinifolia (V) KilpisjaÈrvi (F), 1997 Pontopristia amentorum (FoÈrster) S. borealis (V) KilpisjaÈrvi (F), 1997 Amauronematus eiteli (Saarinen) S. pentandra (S) Parikkala (F), 1998 1. Leaf fold/roll (11) Phyllocolpa nudipectus (Vikberg) S. phylicifolia (V) Joensuu (F), 1996 Phyllocolpa leucosticta (Hartig) S. caprea (V) Puhos (F), 1997 Phyllocolpa puella (Thomson) S. fragilis (S) Joensuu (F), 1997 Phyllocolpa excavata (Marlatt) S. pentandra (S) Joensuu (F), 1997 Phyllocolpa coriacea (Benson) S. aurita (V) MekrijaÈrvi (F), 1997 Phyllocolpa anglica (Cameron) S. dasyclados (V) Krasnojarsk (R), 1993 2. Leaf blade gall (3±5) Pontania proxima (Lepeletier) S. alba (S) Joensuu (F), 1991 Pontania triandrae (Benson) S. triandra (S) Keminmaa (F), 1997 2? Sausage gall (4±10) Pontania dolichura (Thomson) S. phylicifolia (V) PaanajaÈrvi (R), 1996 Pontania dolichura (Thomson) S. glauca (C) KilpisjaÈrvi (F), 1997 3. Apical leaf gall (18) Pontania glabrifrons (Benson) S. lanata (V) Kanin Peninsula (R), 1994 Pontania samolad (Malaise) S. lapponum (V) PaanajaÈrvi (R), 1996 Pontania reticulatae (Malaise) S. reticulata (C) Kolguyev Island (R), 1994 Pontania pedunculi (Hartig) S. caprea (V) Lebed-Ozero (R), 1996 Pontania nivalis (Vikberg) S. glauca (C) Kakhovskiy Bay (R), 1994 Pontania hastatae (Vikberg) S. hastata (V) BjoÈrkstugan (S), 1989 Pontania arcticornis (Konow) S. phylicifolia (V) PaanajaÈrvi (R), 1996 Pontania sp. S. schwerinii (V) Ussuri Reserve (R), 1996 Pontania sp. S. gracilistyla (V) Kedrovaja Pad Reserve (R), 1996 Pontania aestiva (Thomson) S. myrsinifolia (V) PaanajaÈrvi (R), 1996 4. Basal leaf gall (8) Pontania lapponica (Malaise) S. lapponum (V) KilpisjaÈrvi (F), 1997 Pontania pustulator (Forsius) S. phylicifolia (V) Joensuu (F), 1994 Pontania polaris (Malaise) S. polaris (C) KilpisjaÈrvi (F), 1997 5. Petiole gall (2±3) Euura testaceipes (Zaddach) S. fragilis (S) Joensuu (F), 1989 Euura venusta (Zaddach) S. caprea (V) HaÈrskiaÈ (F), 1989 6. Stem gall (4±8) Euura atra (Jurine) S. alba (S) Simpele (F), 1988 Euura atra (Jurine) S. lapponum (V) KilpisjaÈrvi (F), 1997 Euura lasiolepis (Smith) S. lasiolepis (V) Flagstaff, Arizona (U), 1997 6? Multilarval stem gall (1) Euura amerinae (Linnaeus) S. pentandra (S) Joensuu (F), 1998 7. Bud gall (3±11) Euura mucronata (Hartig) S. phylicifolia (V) KilpisjaÈrvi (F), 1997 Euura lanatae (Malaise) S. lanata (V) KilpisjaÈrvi (F), 1997 1 Numbers in parentheses indicate numbers of European species according to Price and Roininen (1993), Kopelke (1994), and pers. obs. The numbers are only approximate because the status of many currently recognized species is uncertain. 2 Letters in parentheses indicate the willow subgenus to which the host belongs: S, Salix;C,Chamaetia;V,Vetrix. 3 F, Finland; R, Russia; S, Sweden; U, United States. The purpose of the present study was to obtain a more DNA Extraction, Polymerase Chain Reactions, and reliable view of the evolution of the galling nematines. For Sequencing this, we used DNA sequence data (678 bp) from the mito- Total DNA was extracted from larvae or adult saw¯ies as chondrial cytochrome b gene coupled with a broader taxo- described in Garnery et al. (1991). The DNA was dissolved nomic sample (36 species). The analysis yielded a robust in 20±50 mlH0, depending on the size of the sample. phylogeny that answered many questions left open in the 2 For the polymerase chain reactions (PCR), we used primers previous study and corrected some apparent errors. The new CB-J-10933 and TS1-N-11683 (Simon et al. 1994), which phylogeny was used to infer the evolutionary history of gall- amplify an approximately 750-bp fragment in the cytochrome type changes and host-plant relationships in the nematine b±tRNA-Ser region.
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