152 ENTOMOLOGICALNEWS GYNANDROMORPHISM IN POLLINATING FIG WASPS (HYMENOPTERA: AGAONIDAE)1 R.A. S. Pereira,2A. P. Prado,1and F. Kjellberg4 ABSTRACT: Gynandromorph specimens ofpollinating fig wasps (Hymenoptera: Agaonidae) are reported forthe first time. Gynandromorph individuals ofPegoscapus tonditzi (pollinator ofFicus citrifolia - Moraceae) and Blastophagapsenes (pollinator ofF. carica) were found in galls from which insectshadnot emerged. P. tonditzigynandromorph specimens showed female and maletis- suesdistributed inamosaic overall partsofthe body, butwith thegenitaliapredominantlymascu- line,whileinB.psenestheindividualshadafemalefrontpartandamalehindpart.Thepresenceof gynanadromorphs at low frequencies in two species suggests that they may also occur in other fig waspspecies,buttheiroccurrenceisnotnoticedbecauseoftheirlowfrequencyandbecauseitisnec- essarytocrackopentheclosedgallstofindtheseinsects. KEYWORDS: Agaonidae, pollinatingfigwasps, Hymenoptera,gynandromorphism. Gynandromorphism is described as the simultaneous presence within the same organism of genotypically and phenotypically male and female tissues (Lauge 1985). Gynandromorph forms have been described in several orders of arthropods (Martini et al. 1999). In Hymenoptera, this phenomenon is described within some families, such as,Anthophoridae (Urban 1999),Apidae (Gordh and Gulmahamad 1975), Chalcididae (Haltead 1988), Diprionidae (Martini et al. 1999), Formicidae (Jones and Phillips Jr. 1985), Halictidae (Nilsson 1987), Scelionidae (Huggert 1977) and others cited by Nilsson (1987). The originofthisphenomenon is not completelyknown, but it is generally at- tributed to developmental anomalies. Nilsson (1987) discusses some possible causes ofgynandromorphism in haplodiploid insects such as hymenopterans: 1) eggs that contain two nuclei and the fertilization ofonly one ofthese may pro- duceagynandromorph; 2)polyspermy,bywhichonespermmayfertilizetheegg whileanucleus froma supernumeraryspermmaygiverisetohaploidcells inthe embryo and thus a gynandromorph; 3) accidental meiosis giving rise to haploid cells in a diploid embryo; 4) the opposite event giving rise to diploid cells from haploid ones and 5) accidental loss ofsex-determining loci. Feininization mediatedby Wolbachia in genetically male individuals, although not known in Hymenoptera (Cook and Butcher 1999), deserves more studies. Feminization due to Wolbachia infection is known in Isopoda (Rigaud and Juchault 1993) and was recently reported in Lepidoptera (Hiroki et al. 2002, Ka- geyama et al. 2002). In Isopoda, Wolbachia-mediated feminization leads to the production ofgynandromorph phenotypes (Rigaud and Juchault 1993). In Dip- tera, Wolbachia infectionsmaybedistributedthroughout somatic tissues(Dobson 1Receivedon December20, 2002.AcceptedonJanuary26,2004. :FFCLRP-USP. Departamento de Biologia, CEP 14040-901, Ribeirao Preto/SP, Brazil. E-mail: raspereira(a)yahoo.com.br. 'Unicamp. Depto. de Parasitologia, CP 6109, CEP 13083-970, Campinas/SP, Brazil. E-mail: apprado(>unicamp.br. 4CEFE-CNRS (Centre d'Ecologie Fonctionnelle et Evolutive), Montpellier, France. E-mail: kjellberg(a>cefe.cnrs_mop.fr. MailedonJuly28,2004 Vol. 114. No. 3. May&June2003 153 et al. 1999); thus, in haplodiploid organisms like Hymenoptera, feminization associated with infection ofsomatic tissues could produce a gynandromorph. The genus Ficus (Moraceae) is pollinated by tiny species-specific pollinating wasps belonging to the familyAgaonidae (Ramirez 1970, Wiebes 1979, Herreet al. 1996). Agaonids show a strong sexual dimorphism, with winged females and wingless pale brown males (Figure 1 A-B). Sex-determination is haplodiploid, males developing from unfertilized eggs and females from fertilized ones (Cook 1993). B Figure 1. Pegoscapus tonditii pollinatorofFicus citrifolia. Normal female and male: A- B. Gynandromorph individuals: C- specimen 1 (dorsal), D- specimen 2 (dorsal), E-F- specimen3 (laterals), ft=femaletissue,mt=maletissue,w=wing. B-Fatthesamescale. Scales = 1mm. 154 ENTOMOLOGICALNEWS Among non-pollinating fig wasps, gynandromorphism was described in the genus Psenobolus (Ichneumonoidea, Braconidae) (Ramirez and Marsh 1996) and the gynandromorph specimen helped to associate female and male forms classified before as different species due to the accentuated sexual dimorphism. However, this phenomenon is not described in the literature forfig wasp species belonging to the superfamily Chalcidoidea that includes pollinating fig wasps. Sixgynandromorphspecimens ofthepollinatingspecies,Pegoscapus tonduzi, were found in crops oftwo trees ofFicus citrifolia sampled duringAugust 2001 in the surroundings ofthe Campinas State University campus, Brazil (22 54'S, 47 03'W). Twenty-five syconia ofeach tree were sampled near the wasp emer- gencephase before anywasps had left the fruit. Each syconium was placed indi- vidually in aplastic flask, andall thewaspswere allowedto emergebeforebeing frozen. The gynandromorph individuals were found in galls from which insects had not emerged, suggesting these insects had some viability problems. Gynan- dromorph specimens showed female and male tissues distributed in a mosaic over all parts ofthe body, but with genitalia predominantly masculine (Figure 1 C-F). The external morphology presented female or male traits according to the predominance offemale ormale tissues respectively, including the development ofwings in these thorax parts with female tissues (Figure 1 F). Thisphenomenon seemstoberare, sinceonly sixgynandromorph individuals wereobservedinapproximately600 syconiaor 14,000malesassessedduringthe five-year study. Another interesting point is that all the gynandromorph individ- uals were found in two samples at the same period ofthe year, suggesting per- haps an environmental factor, such as low temperatures, could cause develop- mental interferences in these insects. Gynandromoiphism was also observed, though in a slightly different form in Blastophagapsenes, the wasp pollinating F. carica. In 1984, fourgynandromorphic individuals were observed in a sample of 127 syconia containing 3,312 males. They were all in non-exited galls, sug- gesting again a lack ofviability. InB. psenes, the individuals had a female front partandamalehindpart. Threewere foundon onetreewithinthe same cropthat matured in May (two in the same syconium), while the fourth was observed on another tree in a crop that matured in July. No gynandromorphic male was observed in other years ofsampling. The presence ofgynanadromorphs at low frequencies in two species suggests thattheymayoccurinotherfigwasp species, buttheiroccurrences isnotnoticed because of their low frequency and because it is necessary to crack open the closed galls to find these insects. More studies will be necessary to elucidate the factors that lead to the development ofgynandromorph fig wasp individuals. ACKNOWLEDGMENTS Wethank J. Cook, S.A. West, andtwo anonymous referees forthe critical reviewofthemanu- script. R.A. S. PereirawassupportedbyFapesp(studentshipno: 98/05067-4). Vol. 114,No. 3, May&June2003 155 LITERATURE CITED Cook,J. M. 1993. SexdeterminationintheHymenoptera: areviewofmodelsandevidence. Here- dity 71:421-435. Cook,J.M.andR.D.J. Butcher 1999. ThetransmissionandeffectsofWolbachiabacteriainpar- asitoids. Researcheson Population Ecology41:15-28. Dobson,S.L.,K. Bourtzis, H. R. Braig, B. F.Jones,W.G.Zhou, F. 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