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The Structure of Cynipid Oak Galls: Patterns in the Evolution of an Extended Phenotype

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The Structure of Cynipid Oak Galls: Patterns in the Evolution of an Extended Phenotype The structure of cynipid oak galls: patterns in the evolution of an extended phenotype Graham N. Stone1* and James M. Cook2 1Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK ([email protected]) 2Department of Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, UK Galls are highly specialized plant tissues whose development is induced by another organism. The most complex and diverse galls are those induced on oak trees by gallwasps (Hymenoptera: Cynipidae: Cyni- pini), each species inducing a characteristic gall structure. Debate continues over the possible adaptive signi¢cance of gall structural traits; some protect the gall inducer from attack by natural enemies, although the adaptive signi¢cance of others remains undemonstrated. Several gall traits are shared by groups of oak gallwasp species. It remains unknown whether shared traits represent (i) limited divergence from a shared ancestral gall form, or (ii) multiple cases of independent evolution. Here we map gall character states onto a molecular phylogeny of the oak cynipid genus Andricus, and demonstrate three features of the evolution of gall structure: (i) closely related species generally induce galls of similar structure; (ii) despite this general pattern, closely related species can induce markedly di¡erent galls; and (iii) several gall traits (the presence of many larval chambers in a single gall structure, surface resins, surface spines and internal air spaces) of demonstrated or suggested adaptive value to the gallwasp have evolved repeatedly. We discuss these results in the light of existing hypotheses on the adaptive signi¢cance of gall structure. Keywords: galls; Cynipidae; enemy-free space; extended phenotype; Andricus layers of woody or spongy tissue, complex air spaces within 1. INTRODUCTION the gall, and surface coats of sticky resins, hairs or spines. Galls are plant tissues, induced by another organism, Mature galls formed by members of the same genus may which provide that organism with food and a measure of also di¡er enormously in size and colour. A long-standing physical protection (Cornell 1983; Price et al. 1987). Oak challenge in understanding the evolution of gall structure gallwasps (Hymenoptera: Cynipidae, tribe Cynipini) has been to explain why such a diversity of morphologies induce the most structurally complex and diverse galls may be found at the same time on the same part of the known of any gall-inducing group (Dreger-Jau¡ret & same host oak species (Askew 1984; Price et al. 1987). Shorthouse 1992; Rohfritsh 1992). Cynipid gall structures Considerable debate surrounds the possible signi¢cance are characteristic of the gall inducer, rather than of the of gall structures, and both non-adaptive and adaptive host-plant (Ambrus 1974; Rohfritsch 1992), and result hypotheses for the genesis of gall diversity have been from cynipid traits expressed at two stages in the wasp's proposed (Cornell 1983; Price et al. 1987; Crespi & life cycle. Morphogens (as yet uncharacterized), which Worobey 1998). If some gall structures evolve more often are probably secreted by the larva, are thought to control than others (perhaps as an emergent property of the devel- the type and structure of plant tissues forming the gall opmental processes involved in gall formation), but go (Rohfritsh 1992), whereas the ovipositional behaviour of extinct at random, sets of gall morphologies could evolve the female determines how many larvae develop within a without selection acting on gall shape. Several adaptive single gall. Gall structures, although constructed of plant alternatives have been proposed. Gall structure may a¡ect tissues, thus represent the extended phenotypes of gall- the ability of galls to protect the gall inducer from £uctua- wasp genes (Stern 1995; Crespi et al. 1997). tions in abiotic conditions, or a¡ect the allocation of Structurally, cynipid galls can be divided into two parts: nutrients to gall tissues (and hence to growth of the gall the larval chamber and the outer gall. The larval chamber, inducer) by the host-plant (Cornell 1983; Price et al. 1987; which is structurally similar in all cynipid galls (Bronner Bagatto et al. 1996; Crespi & Worobey 1998). There is a 1992), is lined with nutritive plant tissues on which the general consensus, however, that the strongest selection larva feeds, and is surrounded by a thin wall of pressure acting on gall form (with the exception of thrips sclerenchyma. The cynipid larva completes its entire galls (Crespi & Worobey 1998)) is probably associated development within this chamber. The diversity of cynipid with avoidance of mortality in£icted by natural enemies. galls is the result of variation in gall tissues that develop The greatest cause of gallwasp mortality occurring after outside the larval chamber. These include surrounding successful gall formation results from attack by two groups of wasps (chalcid parasitoids and inquiline cynipids), which reach the gallwasp by penetrating the gall with a drilling *Author for correspondence. ovipositor (Askew 1965, 1984; Washburn & Cornell 1981; Proc. R. Soc. Lond. B (1998) 265, 979^988 979 & 1998 The Royal Society Received 5 January 1998 Accepted 13 February 1998 980 G. N. Stone and J. M. Cook Evolution ofgall structure in oak gallwasps Cornell 1983; Scho« nrogge et al. 1995, 1996). High mortality whether phylogenetic patterns allow us to infer ancestral of gall inducers can also be caused by vertebrate predators, states for sexual and asexual generation galls in this genus. which also reach the gall inducer by removing the gall wall (e.g. Abrahamson et al. 1989; Cso¨ ka 1997). Gall structures therefore represent the interface through which the gall 2. MATERIALS AND METHODS inducer and two principal causes of mortality interact. (a) Study species Gall traits reducing gallwasp mortality in£icted by natural Collection locations, type of material used in DNA extraction, enemies, and which are under the control of cynipid genes, and character values for each generation of the species studied are should spread through natural selection, and defence is the given in table 1.We selected 28 European Andricus species (38% of commonest function attributed to gall traits (Cornell 1983; all European Andricus) representing the principal structural types Askew 1984; Price et al. 1987). To date, however, the impact present in the genus (described below). Of the selected species, 12 on survivorship of only a few gall characters (diameter, have both sexual and asexual generations in their life cycle,14 have hardness and recruitment of ant guards through nectar only a known asexual generation, and two species have only a secretion) has been demonstrated, and the role of the known sexual generation. Gall structures are known for the majority remains unknown (Washburn 1984; Weis et al. generations given of each species except for the sexual generation 1985; Price & Clancy1986; Abe1992; Stiling & Rossi1996). of A. viscosus, for which the sexual adult female is known, but whose In addition to this structural diversity, a characteristic of gall has yet to be identi¢ed. The asexual generation galls of the cynipid oak galls is that all of the outer gall characteristics selected Andricus species develop on Quercus petraea, Q. pubescens or mentioned above are shared by sets of sympatric species Q. robur, while sexual generation galls develop either on these (e.g. Weld 1960; Ambrus 1974; Askew 1984). This prompts species or on Q. cerris (Ambrus 1974). Many of the galls, two fundamental questions. particularly of the asexual generations, develop on more than one closely related oak species (Ambrus 1974). In all cases, the galls 1. What are the phylogenetic relationships between gall- have the same structure (in terms of the character states used wasps inducing structurally similar galls? Is the here) on all alternative hosts (Ambrus 1974). evolution of novel gall structures a rare event in oak To check the monophyletic status of Andricus, we have included cynipid evolution, such that phylogenetic proximity and in our analysis ¢ve species from other oak cynipid genera: Aphe- similarity in gall structure are highly correlated, or have lonyx cerricola Gir., Biorhiza pallida Oliv., Cynips cornifex Htg., Cynips certain gall traits evolved independently many times? divisa Htg., and Cynips quercus Fourcr. To allow tree rooting we 2. What underlying processes have generated the observed also included Diplolepis rosae Htg. in the tribe Rhoditini, the patterns? sister group to the Cynipini/Pediaspini clade (Ronquist 1995; Here we address the ¢rst question by examining the Liljeblad & Ronquist 1997). distribution of gall traits across the phylogeny of a selected group of oak gallwasp species. We then consider the (b) Scoring gall character states patterns we observe in the light of existing non-adaptive We map three binary characters and one multistate character and adaptive hypotheses for the evolution of gall structure. across our oak cynipid phylogeny (table 1). Character states are The selected oak gallwasp taxon for study is the genus illustrated for representative examples in ¢gure 1. The binary Andricus, which includes the most complex and diverse traits are as follows. oak cynipid galls. We present a molecular sequence phylo- 1. Gall surface covered in sticky resin or not sticky. geny for 28 members of the genus, which constitute clear 2. Gall surface smooth or bearing spines (compare ¢gure 1a d, m sets of species sharing similar gall morphology (¢gure 1). ^ with ¢gure 1n,q). We test the null hypothesis that gall traits are randomly 3. Gall single chambered or multichambered (compare ¢gure 1a distributed through the gallwasp phylogeny and ask (i) ^ d with ¢gure 1e s). which traits, if any, are conserved within clades; (ii) ^ Overall gall structure is a multistate character with seven which traits, if any, have evolved repeatedly in indepen- states, and is scored separately for sexual and asexual genera- dent lineages; and (iii) how rapidly (in terms of sequence tions where both are present.
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