25 Oct 2001 17:34 AR ar147-11.tex ar147-11.sgm ARv2(2001/05/10) P1: GJBAnnu. Rev. Entomol. 2002. 47:299–330Copyrightc! 2002 by Annual Reviews. All rights reservedHOW TO BE A FIG WASPGeorge D. WeiblenUniversity of Minnesota, Department of Plant Biology, St. Paul, Minnesota 55108;e-mail: [email protected] Words Agaonidae, coevolution, cospeciation, parasitism, pollination■ Abstract In the two decades since Janzen described how to be a fig, more than200 papers have appeared on fig wasps (Agaonidae) and their host plants (Ficus spp.,Moraceae). Fig pollination is now widely regarded as a model system for the study ofcoevolved mutualism, and earlier reviews have focused on the evolution of resourceconflicts between pollinating fig wasps, their hosts, and their parasites. Fig wasps havealso been a focus of research on sex ratio evolution, the evolution of virulence, coevolu-tion, population genetics, host-parasitoid interactions, community ecology, historicalbiogeography, and conservation biology. This new synthesis of fig wasp research at-tempts to integrate recent contributions with the older literature and to promote researchon diverse topics ranging from behavioral ecology to molecular evolution.CONTENTSINTRODUCING FIG WASPS ........................................... 300FIG WASP ECOLOGY ................................................. 302Pollination Ecology .................................................. 303Host Specificity ..................................................... 304Host Utilization ..................................................... 305Sex Ratio .......................................................... 305Gallers, Parasitoids, and Predators ...................................... 307FIG WASP SYSTEMATICS ............................................. 308Phylogenetic Relationships ............................................ 310Morphological Apomorphies ........................................... 311FIG WASP EVOLUTION ............................................... 312Modes of Speciation ................................................. 312Coadaptation ....................................................... 316Resource Conflicts ................................................... 317Dioecious Fig Conflicts ............................................... 318Molecular Evolution ................................................. 319BEYOND FIG WASPS ................................................. 3200066-4170/02/0101-0299$14.00299Annu. Rev. Entomol. 2002.47:299-330. Downloaded from arjournals.annualreviews.orgby UNIVERSITY OF MARYLAND - COLLEGE PARK - MCKELDIN LIBRARY on 03/02/10. For personal use only.25 Oct 2001 17:34 AR ar147-11.tex ar147-11.sgm ARv2(2001/05/10) P1: GJB300 WEIBLENINTRODUCING FIG WASPSThe family Agaonidae (Hymenoptera: Chalcidoidea) includes several hundredparasitic wasp species that are closely associated with the fig inflorescence, anenclosed receptacle (or syconium), that characterizes the genus Ficus (Moraceae).All fig wasps are confined to figs as larvae, and their specialized diets are re-stricted to fig embryos, galled fig ovaries, or other fig wasp larvae (15). The lifehistories of these diminutive wasps include a fascinating variety of ovipositionmodes and host interactions, running the gamut from mutualism to antagonism.Molecular phylogeny suggests that the pollination mutualism evolved once andcharacterizes the subfamily Agaoninae (111). These pollinators of figs (Figure 1)show peculiar morphological adaptations, extreme host specificity, and life cy-cles that are tightly synchronized with fig phenology (177). The mutualism hasbeen the source of much speculation on the nature and extent of the coevolu-tionary processes involved (133, 135, 177, 182). Comparative phylogenetic stud-ies are possible now that phylogenies are available for fig wasps globally (111),and for Neotropical (112), Afrotropical (101) and Indo-Pacific fig pollinators(161). The first comparative studies based on molecular data have examinedevolutionary hypotheses including coadaptation with host plants (159), male di-morphism (46), female virginity (165), and Hamilton’s theory of kin selection(168).Interest in fig wasps, as reflected in the number of publications, has also in-creased dramatically since Janzen (95) described how to be a fig more than twodecades ago (Figure 2). The lifelong contribution of J.T. Wiebes also provided ataxonomic foundation for fig wasp research today. Although many hundreds offig wasp species have yet to be described, advances in ecology and evolution haveoutpaced systematic studies, with international symposia held every few years(25, 34, 47). Earlier reviews have focused on evolutionary conflicts arising fromthe fig pollination mutualism (1, 4, 22), fig wasp biology in India (2) and Panama(85), and the similarity of fig wasp interactions to species interactions in general(86, 87, 200). The following review summarizes our current state of knowledgeabout fig wasps in an attempt to correct misconceptions in the older literature andto promote research on fig wasp behavior, ecology, taxonomy, phylogenetics, andevolution.−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→Figure 1 Pollinating fig wasps (Agaoninae: Agaonidae). (a) Oligocene Tetrapus fromFlorissant, Colorado (28). (b) Extant Tetrapus from Santa Catarina, Brazil. (c) Ventralview of the female head in Kradibia ohuensis showing mandibular appendage with sixlamellae (scale = 0.1 mm). (d ) Pollen pocket of Ceratosolen kaironkensis containingFicus microdictya pollen grains. (e) Four-legged Wiebesia frustrata male with atrophiedmidleg. ( f ) Kradibia ohuensis male with vestigal eyes and dorsal spines on head(scale = 0.1 mm).Annu. Rev. Entomol. 2002.47:299-330. Downloaded from arjournals.annualreviews.orgby UNIVERSITY OF MARYLAND - COLLEGE PARK - MCKELDIN LIBRARY on 03/02/10. For personal use only.25 Oct 2001 17:34 AR ar147-11.tex ar147-11.sgm ARv2(2001/05/10) P1: GJBHOW TO BE A FIG WASP 301Annu. Rev. Entomol. 2002.47:299-330. Downloaded from arjournals.annualreviews.orgby UNIVERSITY OF MARYLAND - COLLEGE PARK - MCKELDIN LIBRARY on 03/02/10. For personal use only.25 Oct 2001 17:34 AR ar147-11.tex ar147-11.sgm ARv2(2001/05/10) P1: GJB302 WEIBLENFigure 2 Numbers of publications on (a) fig wasp systematics, (b) evolution, and (c)ecology prior to 1960 and during