Butll. Inst. Cat. Hist. Nat., 71: 83-95. 2003 ISSN: 1133-6889 GEA, FLORA ET FAUNA The life cycle of hispanicus (Hartig, 1856) n. stat., a sibling species of A. kollari (Hartig, 1843) (: Cynipidae)

Juli Pujade-Villar*, Roger Folliot** & David Bellido*

Rebut: 28.07.03 Acceptat: 01.12.03

Abstract and so we consider A. mayeti and A. niger to be junior synonyms of A. hispanicus. Finally, possible causes of the speciation of A. kollari and The marble gallwasp, , common A. hispanicus are discussed. and widespread in the Western Palaeartic, is known for the conspicuous globular caused by the asexual generations on the of several KEY WORDS: Cynipidae, Andricus, A. kollari, A. species. The sexual form known hitherto, hispanicus, biological cycle, sibling species, formerly named Andricus circulans, makes small sexual form, speciation, distribution, morphology, gregarious galls on the buds of Turkey oak, A. mayeti, A. burgundus. ; this oak, however, is absent from the Iberian Peninsula, where on the other hand the cork oak, Q. suber, is present. Recent genetic studies show the presence of two different Resum populations or races with distribution patterns si- milar to those of Q. cerris and Q. suber. We present new biological and morphological Cicle biològic d’Andricus hispanicus (Hartig, evidence supporting the presence of a sibling 1856) una espècie bessona d’A. kollari (Hartig, species of A. kollari in the western part of its 1843) (Hymenoptera: Cynipidae) range (the Iberian Peninsula, southern France and North Africa), Andricus hispanicus n. stat.. Biological and morphological differences separating these Andricus kollari és una espècie molt comuna dis- two species from other closely related ones are tribuida a l’oest del paleartic coneguda per la given and the new sexual form is described for the gal·la globular i relativament gran de la generació first time. This form of A. hispanicus, causing assexual que es localitza als borrons de diverses isolated galls in Q. suber, is identical to espècies de roure. La forma sexual coneguda fins Andricus mayeti n. syn. and Andricus niger n. syn. avui, denominada Andricus circulans, provoca petites gal·les gregaries als borrons del roure turc Quercus cerris, (aquest roure no es troba a la pe- * Universitat de Barcelona. Facultat de Biologia. Departament nínsula Ibèrica, on si que hi ha Q. suber). Recents de Biologia . Avda Diagonal 645. E-08028 Barcelona, estudis genètics mostren la presència de dues Spain. E-mail: [email protected] ** Université de Rennes 1. Faculté Sciences. C.N.R.S. poblacions o races diferents amb un patró de UPRES- A 6026. Équipe Canaux Récepteurs Membranaires. distribució similar al de Quercus cerris i al de Q. Bât 13-Campus de Baulieu. 35042-Rennes Cedex - France. suber. En aquest estudi presentem evidències bio-

83 GEA, FLORA ET FAUNA lògiques i morfològiques que posen de manifest la forma es idéntica a Andricus mayeti (= Andricus presència d’una espècie bessona d’Andricus kolla- niger syn. n.), así pues consideramos Andricus ri en la zona oest d’Europa (península Ibèrica, sud mayeti como nueva sinonimia de Andricus de França i nord d’Àfrica), Andricus hispanica hispanica. Para finalizar, se discuten las razones status n. Es descriuen les diferències biològiques i que pudieron ocasionar la separación específica morfològiques que permetran separar aquestes entre Andricus kollari y A. hispanica. dues espècies d’altres espècies molt properes, i es descriu per primer cop la forma sexuada d’Andri- PALABRAS CLAVE: Cynipidae, Andricus, A. kollari, cus hispanica que ocasiona gal·les aïllades als A. hispanicus, ciclo biológico, especies geme- borrons de Quercus suber. Aquesta forma és idèntica a Andricus mayeti (= Andricus niger syn. las, forma sexual, especiación, distribución, n.), així doncs considerem Andricus mayeti com a morfologia, A. mayeti, A. burgundus. nova sinonimia d’Andricus hispanica. Per acabar, es discuteixen les raons que van poder ocasionar la separació específica d’Andricus kollari i A. Introduction hispanica.

MOTS CLAU: Cynipidae, Andricus, A. kollari, A. The marble , Andricus kollari, is hispanicus, cicle biològic, espècies bessones, one of the best known cynipids and has forma sexual, especiació, distribució, morfolo- received great attention in the literature gia, A. mayeti, A. burgundus. because of its interesting and complex life cycle and conspicuous unisexual galls. In former times these galls were collected for Resumen industrial purposes for their high tannin content. The dry substance can consist of up to 65 % Ciclo biológico de Andricus hispanicus tannins, and this substance was used for (Hartig, 1856) una especie gemela de A. leather or producing ink (Kieffer, kollari (Hartig, 1843) (Hymenoptera: Cyni- 1897-1901). The native range of the species is pidae) divided geographically between south- western Europe (mostly the Iberian Penin- Andricus kollari, es una especie muy común dis- sula) and eastern Europe, although human tribuida en el oeste del paleártico, conocida por la introduction of the host of the sexual gene- agalla globular y relativamente grande de la gene- ración asexual producida en yemas de varias espe- ration, Quercus cerris (Turkey oak), has cies de roble. La forma sexual conocida hasta hoy, favoured its dispersal over northern and denominada Andricus circulans, provoca peque- north-western Europe (Schönrogge et al., ñas agallas gregarias en yemas del roble turco 1998), where it is now one of the most easily Quercus cerris, (este roble no se encuentra en la Península Ibérica, donde si hay Q. suber). Recien- found species at many sites. tes estudios genéticos mostraron la presencia de Beijerinck (1902) described the life cycle dos poblaciones o razas distintas con un patrón de of this species, and later Marsden-Jones distribución similar al de Quercus cerris y al de Q. (1953) and Folliot (1964) confirmed it. There suber. En este estudio presentamos evidencias biológicas y morfológicas que ponen de manifies- is a conspicuous unisexual generation forming to la presencia de una especie gemela de Andricus spherical monolocular bud galls (10-30 mm kollari en la zona oeste de Europa (Península Ibé- in diameter) on various species of Quercus rica, parte sur de Francia y Norte de África), Andricus hispanica status n. Se describen estas dife- subgenus Quercus while the bisexual gene- rencias biológicas y morfológicas que permitirán ration forms small gregarious galls in buds of separar estas dos especies de otras especies muy Q. cerris. Some authors have proposed that A. cercanas, y se describe por primera vez la forma kollari might reproduce without a sexual sexual de Andricus hispanica, que ocasiona aga- llas aisladas en las yemas de Quercus suber. Esta generation in its lifecycle in regions where Q.

84 cerris is either rare (such as the Transcar- doubt of the A. kollari type, and the adults pathian region of the Ukraine: Melika & obtained confirmed this observation. This ex- Csóka, 1993; Csóka, 1997) or entirely absent periment has been mentioned previously in (Iberia: Nieves-Aldrey, 1987; Csóka et al., Pujade-Villar (1992) and showed that although 1998; Dajoz, 1999). Pujade-Villar (1992) Q. cerris is absent from the Iberian Peninsula, reported the presence of a sexual generation the so-called Iberian A. kollari have an alter- in Iberian populations, although it was not nating life cycle in this area. As mentioned in described because only the sexual female was Pujade-Villar (1991), this sexual form is found. slightly different from the sexual form of Recent genetic results using allozyme data eastern A. kollari (formerly called A. circu- (Stone et al., 2001) support the presence of a lans); the relationship between the agamic sexual generation in Iberian populations and form (A. kollari) and the sexual form (A. suggest a genetic isolation between the circulans) was established by experimental eastern and western populations. According studies by Benson (1953). The two specimens to the results the eastern and western forms of from Montseny mentioned above were compa- A. kollari would have differentiated completely red with: a) adults emerged from sexual galls between 1 and 2 million years ago and have to found on Q. suber attributed to A. mayeti; b) a series of adults reared from them, because of be considered separate species. The western their high similarity; c) sexual galls of eastern form is found in the Iberian Peninsula, A. kollari obtained experimentally by R.F. in extending into south-west France, while the the north of France. Finally it was also eastern form occurs in eastern Europe, compared with other sexual forms of the including the Italian and Balkan peninsulas, kollari group (see Folliot et al., 2003). as well as in north and north-western Europe. Biological experiments with both Spanish It is very interesting that the distribution of and Northern French populations were also this western form shows a close coincidence carried out over several years. A large number with the distribution of Q. suber (cork oak), of unisexual galls collected in Spain and an oak closely related to Q. cerris. supposedly linked to Q. suber were brought The present study describes the discovery to France, where unisexual females were of the sexual male of the Iberian form and the reared for experiments on Q. cerris (R.F.), identification of the host of the sexual while northern French unisexual galls were generation as Q. suber, so that the redescrip- taken to Spain, where experiments on Q. tion of the western form of A. kollari as a new suber were performed (J. P.-V.). species can now be made. We follow the current terminology of morphological structures (Gibson, 1985; Ronquist & Nordlander, 1989), surface sculp- Material and methods turing is given after Harris (1978). Measu- rements and abbreviations used here include: Two sexual females of Andricus were POD (post-ocellar distance) is the distance found ovipositing in buds of Q. pubescens on between the inner margins of the posterior Montseny in the north-east of the Iberian ocelli; OOD (ocellar-ocular distance) is the Peninsula on 18th April 1987. The branch distance from the outer edge of a posterior where the females were found was kept inside ocellus to the inner margin of the compound a sleeve until July 1987; the galls obtained eye; COD is the distance between lateral and (one for each sexual female) were beyond frontal (central) ocellus.

85 GEA, FLORA ET FAUNA

Results Thus it would appear that the sexual form of western A. kollari is A. mayeti, and a Two sexual females of Andricus were description of the new species can now be found ovipositing on Q. pubescens and the made. This should be called Andricus branch was kept in a sleeve. The agamic hispanicus (Hartig, 1856) n. stat., since it was generation that developed turned out to be A. Hartig who first described galls of A. kollari kollari (Pujade-Villar, 1992). These females from the south of Spain (in the Sierra de Ron- of the sexual form of Iberian A. kollari were da) and thus inside the Iberian native range morphologically identical to adults obtained (Pujade-Villar & Bellido, 2000). Considering from A. mayeti galls on Q. suber, except for A. circulans to be the sexual form of A. minor differences falling within the range of hispanicus (i. e. Iberian Andricus kollari) as intraspecific variation. Nieves-Aldrey (2001) does is mistaken The ephemeral and inconspicuous bud (Pujade-Villar, 1991; 1992; 1997), especially galls of A. mayeti on Q. suber are normally when Q. cerris is not found in the Iberian isolated or in pairs; sexual adults are of a Peninsula; a new sexual form for A. black colour with a striated mesopleuron, but hispanicus needs to be described. with several clear morphological and biolo- gical differences from the sexual form of Andricus hispanicus (Hartig, 1856) n. stat. eastern A. kollari. Cynips hispanica Hartig, 1856. Agamic gall Biological experiments showed that whereas Cynips kollari var minor Kieffer, 1897-1901. unisexual females from Brittany (now known Agamic form to be of eastern origin) quickly inspected and Cynips kollari minor (Kieffer) Dalla Torre & oviposited into buds of Q. cerris, they Kieffer, 1910 (syn. in Bellido, Ros-Farré, showed no interest in Q. suber. Unisexual Melika & Pujade-Villar, 2003) females of A. kollari collected in Spain Andricus hispanica (Hartig) Pujade-Villar & showed the reverse behaviour: when left on Bellido, 2000 after Benson, 1953. Q. cerris branches they showed no interest in Andricus mayeti Kieffer, 1896. Bull. Soc. them and died before laying any eggs on the Entomol., France: 370 (sexual female and wrong host, while on Q. suber they showed gall) n. syn. an active oviposition behaviour. Despite the Andricus luteicornis var niger Kieffer, 1901. large number of unisexual females observed, Ann. Soc. Entom. France, 70: 453 (sexual oviposition on the wrong host only excep- gall) n. syn. tionally occurred and no galls developed in Andricus l. var niger Tavares, 1902 Brotéria, these cases (R.F.). In any case, this oviposi- tion into an oak species other than the usual 1: 104 (male, female and gall); homonymy host can be induced at a low rate in the with Kieffer, 1901 n. syn. laboratory when females are given no choice, Andricus niger Tavares, 1916. Brotéria Sér although no galls were observed to develop in zool., 14: 84 n. syn. such cases (e.g. the oviposition of the sexual form of A. kollari on Q. robur (Marsden- Jones, 1953) or on Q. ilex, Q. pubescens and Redescription of the sexual form Q. robur (Folliot, 1964); the latter author also reported the sexual form of A. kollari Type material: The type material from the ovipositing on Q. ilex, but no agamic galls Kieffer collection has been lost. were ever found). Material studied– Experimental material: 2

86 12

34

5 6

FIGURES 1-6. Morphological aspects of the sexual form of Andricus hispanicus (A. mayeti). Head in dorsal view (1), head and mesosoma in lateral view (2), head in frontal view (3), mesosoma in dorsal view (4), propodeal area (5) and gall (6). females ovipositing on Quercus pubescens; 7 Length: 1.7-2.0 mm (for males and females). males and 12 females obtained from galls Colour– All the body black. Wing veins dark collected in several localities of the province brown. Some specimens with brown antennae, of Barcelona (north-east Spain). All material instead of black. deposited at Barcelona University. Female head (Figs 1, 3): Without pubescence;

87 GEA, FLORA ET FAUNA in dorsal view around 2.09-2.36 times as wide Metascutellum sculptured. Lateral carinae of as long and in frontal view 1.13 times as high propodeum thin, of a uniform thickness, only as wide. Genae coriaceous-alutaceous, not slightly bowed outwards, internal area broadened behind compound eyes. POD twice smooth and shiny (a weak median carina is OOD; OOD 1.4 times lateral ocellus diameter present in the lower part of the propodeal and more or less equal to COD (ratio area). Wings hyaline. Forewing margin with POD:OOD:COD:lateral ocellus diameter is short and scattered setae on its anterior 22:10:10:7). Coriaceous-alutaceous sculpture. margin; radial cell 5.0 times as long as broad; Clypeus conspicuous and suboval in shape. 2r vein angled. Areolet normally conspi- Face with only some very short and weak cuous. Tarsal claws with an acute basal lobe irradiating striae around clypeus, never and forming an acute angle. Anterior tibiae reaching either antennal toruli or compound provided with only a few short and applied eye margin. Transfacial line more or less hairs. equal to eye height. Diameter of toruli more Female metasoma: Slightly shorter than or less 1.5 times their separation and slightly head plus mesosoma together; without pubes- longer than distance between toruli and eye cence except at the base of the 2nd metasomal margin. Antenna with 13 segments, 0.8 times tergite. Ventral spine of hypopygium around 3 as long as body or slightly longer; pedicel 2.0 times longer than broad, with sparse setae not times as long as wide; first flagellomere 1.2 forming an apical tuft; when the adult is dried times as long as the second and 1.6 times as this relative length of hypopygial spine is long as the pedicel; subsequent flagellomeres lower (around 1-2 times) because both valves gradually decreasing in length, later flagello- open longitudinally. meres longer than wide and the last more or Male: Same as female, but antenna with 14 less twice as long as wide. segments, the third one curved, dorsally Female mesosoma (Figs 2-5): Without flattened, proximally excavate and distally pubescence except for some hairy zones on expanded, and with weaker sculpture, more the propodeum, with coriaceous-alutaceous alutaceous. sculpture. Notauli complete, anteriorly less Distribution: Iberian Peninsula, southern impressed, posteriorly convergent and wide, France, but probably also in North Africa, delimiting an area with regular closely always near to its host, Quercus suber. The reticulate-alutaceous sculpture and not Corsican record (Pujade-Villar et al., 2000) longitudinally striated. Median scutal line ab- must be regarded as provisional because the sent. Mesopleuron completely striated, with agamic form was not collected (Villeman some striation also on lateral inferior margin pers. comm.); the agamic gall was not found of pronotum. Circular scutellum, only slightly although is very easy to detect. wider than long, with weak reticulated Gall (Fig. 6): Similar to other sexual galls of sculpture, less evident in the central part the Andricus kollari group. A small bud gall usually delimited by two divergent carinae, (1.5 × 1.2 mm) on Quercus suber, isolated or marginated laterally and not lobed posteriorly. in pairs (unlike those of A. circulans or A. Scutellar foveae oval, disposed transversely, larshemi), with its basal part hidden from smooth, shiny and not pubescent inside, not view by bud-scales and apical part (covering delimited posteriorly by a carina and sepa- 1/3 to 1/2 of the gall) projecting outside. The rated from each other by a septum. Metanotal surface of the gall is of a yellowish to brown foveae elongated and interiorly pubescent. colour, nearly smooth, with no striation,

88 8

7

10 9

12 11

FIGURES 7-12. Morphological aspects of the sexual form of Andricus kollari sensu stricto (A. circulans) (7, 9, 11) and A. burgundus (8, 10, 12). Mesosoma in dorsal view (7-8) and in lateral view (9-10). Head in dorsal view (11-12). (Figures 7, 9 and 11 are also available at http://morphbank.ebc.uu.se, as well as other images.)

89 GEA, FLORA ET FAUNA without pubescence; the gall is ovoid and hispanicus (Figs. 7 and 4, respectively); in the more or less conical, the tops are pointed, and shape of the scutellum, oval and convex in A. the gall wall is very thin. Galls appear in kollari, rounded and less convex in A. March or April and adults emerge shortly hispanicus (Figs. 7 & 11 and 4 & 2, respecti- afterwards through a large round lateral vely); and in the galls (in groups on Quercus opening below the top. cerris in A. kollari and isolated or in pairs on Taxonomic comments: Kieffer (1901) descri- Q. suber in A. hispanicus). bed galls of Andricus luteicornis var niger However, in the unisexual generation the from information given by Tavares. Tavares adults and the galls of the two species are im- (1902) described the male and redescribed the possible to separate morphologically (Bellido gall of this variety, entering inadvertently into et al., 2003). Certainly other species in the A. homonymy with Kieffer’s name. Later on kollari group are very similar morpholo- Tavares (1916) considered the variety to be a gically and for a long time many of the unise- different species. A. niger has been recorded xual adults of the species of this group were from Portugal and Spain (Nieves-Aldrey, impossible to separate (Kieffer, 1897-1901; 2001) and from Corsica (Pujade-Villar et al., Dalla Torre & Kieffer, 1910; Tavares, 1931) 2000), although in retrospect this latter but the galls are very different. The case of reference must be treated with caution. The the western and eastern forms of A. kollari descriptions of the galls and adults of A. sensu lato is somewhat different, since no mayeti Kieffer and A. niger are identical morphological differences can be found and (Pujade-Villar, 2002), as are the distributions moreover the galls are identical. Thus A. of the two species. The only difference is in hispanicus and A. kollari must be considered the relative length of the hypopygial spine sibling species that can only be separated by (Kieffer, 1897-1901: 397 & 420; Kieffer, biology and by the sexual adults and their 1902: 559), but this difference falls within the galls. range of intraspecific variation. Therefore we As regards other previously described se- consider A. niger Kieffer, 1901, to be a new xual forms in the A. kollari group (Docters synonym of A. mayeti Kieffer, 1896 and thus van Leeuwen, 1956; Docters van Leeuwen & also of A. hispanicus. Dekhuijzen-Maasland, 1958; Wiebes-Rijks, The sexual form of A. hispanicus (A. 1978), the sexual form of A. hispanicus is mayeti) is very close morphologically to the clearly different from all of them, either in the sexual form of A. kollari (A. circulans) and to galls or in morphological characters mainly A. burgundus Giraud, 1859, only known in its relating to the mesosoma sculpture and sexual form. All of them have a longitudinally notauli. Galls and adults of the sexual form striated mesopleuron, the posterior margin of recently described for A. corruptrix and the the scutellum rounded and a reticulated- sexual form of A. hispanicus are similar but alutaceous sculpture on the scutum. show some clear differences such as the The sexual form of A. hispanicus differs propodeal area and notauli (see Folliot et al., from the sexual form of A. kollari in the form in press). of the notaulus, which is wider and very A. hispanicus is also very close morpholo- conspicuous in A. kollari and shallower gically to A. burgundus, recently redescribed anteriorly and narrower in A. hispanicus by Nieves-Aldrey (2001). However the cha- (Figs. 7 and 4, respectively); in the scutellum racters given by this author are not satis- sculpture, rougher in A. kollari than in A. factory for separating the two species. A.

90 burgundus has narrow notauli clearly found in places very far from Q. suber stands. separated at their base (Fig. 8), while A. The agamic form, which is bigger, would hispanicus has wider and posteriorly conver- have a greater ability to disperse and because gent notauli (Fig. 4), like A. kollari (Fig. 7). of its superior flight capacity would be able to Moreover, the scutellum and scutum sculpture locate Q. suber, the host of the sexual genera- is strongly rugose in A. burgundus (Fig. 8), a tion, in spite of the discontinuous distribution character also present in A. kollari (Fig. 7), of this oak in the Iberian Peninsula (Toumi & while in A. hispanicus the sculpture is much Lumaret, 1998). weaker (Fig. 4); the ocelli are smaller in A. But what was the origin of A. hispanicus? hispanicus; the ratio of OOD to the ocelli Sequence data suggest that the Iberian diameter is bigger in A. burgundus (Fig. 1, population of A. kollari sensu lato began to 12); and the sculpture on the dorsal part of the diverge from the Central European and Balkan head and the lateral part of the thorax is populations 2-4 million years ago, through a weaker in A. hispanicus (Fig. 1, 2) than in the host shift of the sexual generation between Q. other two species (Figs 9-12). The propodeal cerris and Q. suber (probably from Q. cerris carinae in these three species are very similar, to Q. suber) (Stone et al., 2001; Stone, pers. parallel or curved slightly outwards, and comm.). The question is how this shift took cannot be used as diagnostic characters as place. they can with other species of Andricus; Some authors state that host shifts have finally, all three species often show signs of a been rare, especially in the because weak median propodeal carina. of their extreme specialisation and low dispersal abilities (Cornell & Washburn, 1979; Kinsey, 1920), and Cynipini are certainly constrained Discussion by the need to successfully induce galls (Abe, 1988, 1991, 1998; Cook et al., 1998, 2002). The results of our biological experiments However some recent host shifts from wild to clearly show the lack of recognition of Q. domestic roses are known amongst Nearctic cerris by agamic females of A. hispanicus. As Diplolepis (Tribe Rhoditini) (Shorthouse, Stone et al. (2001) suggest, a divergence in 1988, 1994; Shorthouse & Brooks, 1998) and the chemical cues associated with oviposition some authors (Stone et al., 2001) propose that behaviour may have evolved between A. host shifts to Quercus subgenus Cerris from hispanicus and A. kollari sensu stricto. Quercus subgenus Quercus must have occurred. Genetic results also support the presence Host shifts may also occur (or be favoured) as of two clearly differentiated geographical a result of strong selection pressures, such as genotypes within A. kollari sensu lato, closely intraspecific competition or . This corresponding to the distributions of their has been proposed as the mechanism genera- respective sexual form hosts; there was very ting two host races of the gall-inducing little evidence of gene flow (Stone et al., tephritid fly Eurosta solidaginis (Hess et al., 2001). This is also supported by our own 1996; Feder, 1995). However, although parasi- observations, since galls of the sexual gene- toid pressure plays an important role in cynipid ration are found in great numbers locally, population dynamics (Washburn & Cornell, facilitating mating between males and females. 1981; Frankie & Morgan, 1984; Sitch et al., After mating, dispersal of females probably 1988; Plantard et al., 1996), given the takes place, since unisexual galls could be similarity of the galls it seems unlikely that

91 GEA, FLORA ET FAUNA parasitoid-induced pressure would play the refuges as the presence of a mixed region of major role in this case. In the case of A. eastern and western oak genotypes in Central kollari and A. hispanicus it is hard to test this Europe suggests (Ferris et al., 1993). hypothesis, although gall similarity and the Evergreen and other Mediterranean rapid shift of parasitoids from native galls to flora suffered an even greater restriction in invasive species of cynipids make the their distribution, and were reduced to some hypothesis unlikely. localities in the south of the Iberian The present distribution of the two sibling Peninsula, the Eastern Mediterranean and species is explained by the glacial and post- North Africa (Roberts, 1989), mainly in glacial movements of flora and fauna taking suitable microclimates in the mountains place in the Western Palaearctic during the (Willis, 1992, 1994). The conditions in these Pleistocene (Stone et al., 2001). In Europe, refuges were different for each refuge; the mountain ranges hindered the retreat of the Balkans are especially complicated because Arcto-Tertiary forests, which were devastated of their topography, which creates a wide by the cold conditions, so that only some ge- range of environmental variation (Willis, nera survived, oaks amongst them (Collinson, 1994). Quercus cerris and Iberian Q. suber 1988; Sitte et al., 1994). Indeed, a very rapid would have been isolated from each other onset of cold conditions, such as seems to increasingly often as interglacials got cooler. have occurred at times, would have allowed Iberian Q. suber and Q. cerris are not now in no time for the flora to retreat and isolation contact naturally even under interglacial would have quickly occurred, whether there conditions; the contact is an indirect one were mountain ranges in the way or not. Oak through Italian Q. suber, which is rather diversity was greatly reduced, and probably different as Toumi & Lumaret (1998) show. diversity as well, since the Tertiary Geology is another factor limiting the spread oak flora was rich and many species were of Q. suber, since calcareous soils would abundant (Mai, 1995). European cynipid po- have been a barrier to it and may have helped pulations were greatly affected by the repeated to isolate the Iberian and Italian populations glaciations, since they were confined by the from one another. ice sheets, together with their hosts, to Thus recolonisation movements of the oak refuges mainly in the Italian, Balkan and hosts from glacial refuges would explain the Iberian peninsulas but also in North Africa present distribution pattern of the two gall and the Eastern Mediterranean (Collinson, wasp species; Andricus hispanicus would 1988; Roberts, 1989; Delcourt & Delcourt, have reinvaded southern France from its 1988; Bennett et al., 1991; Hewitt, 1996). Iberian refuges and A. kollari sensu stricto Present patterns were established mainly after from Balkan and Italian ones. In Italy, the recolonisation of previously iced regions. although genetic analyses have not detected In Europe, recolonisation from both the east A. hispanicus, since the samples were and the west reunited the oak flora, except for collected in zones without Q. suber, the those oaks remaining in their glacial refuges, presence of this species may yet be confirmed like Q. faginea in the Iberian Peninsula and after the recent discovery of galls apparently Q. cerris, because of its narrower climatic belonging to A. niger, now shown to be the tolerance (Sandor, pers. comm.), in Eastern sexual generation of A. hispanicus, in Corsica Europe. The colonisation of Central Europe (Pujade-Villar et al., 2000), although this re- took place from both eastern and western cord must be considered provisional until

92 more studies are carried out. If this record is Western Palaearctic, both in zones where Q. confirmed, it will imply that A. hispanicus cerris or other closely related oaks are present has spread together with its host and probably (e.g. Eastern Europe and Turkey) and in zo- has the same distribution range, although the nes where the most likely host of the sexual inconspicuousness of the sexual galls and generation is Q. suber (Atkinson, 2000; Meli- their similarity to those of A. kollari sensu ka et al., 2000: Nieves-Aldrey, 2001; Cook et stricto mean that the species remains al., 2002; Rokas et al., 2003). However, each undetected in many places. It would be case must be studied carefully and genetic, interesting to carry out further genetic biological and morphological studies must be analyses of unisexual adults in the contact zo- carried out. Recent genetic studies show nes where both Q. suber and Q. cerris are pre- different lineages of A. quercustozae for each sent, to test whether both species are present. oak glacial refuge, and in this case the Iberian However, the separation of the two species lineage has diverged from other Western seems to be older than the last glaciation, and Palaearctic populations and only shows a although the glaciations were not so intense subset of the ancestral allozyme polymor- 2-4 million years ago (Webb & Bartlein, phism (Rokas et al., 2003). 1992), the presence of significant ice sheets at that time suggests that they probably played some role in the speciation of the two Acknowledgements lineages. Recent studies on allozyme variation in Q. We would especially like to thank Palmira suber and current DNA-based studies at the Ros i Farré (University of Barcelona) for the University of Cambridge (John Parker, pers. SEM pictures illustrating this paper and comm.) show that the Iberian Peninsula is Graham Stone for his valuable comments probably the centre of origin of the species about the genetic data. and supports a higher genetic diversity, and that, as the paleobotanical data corroborate, several cork oak migrations to North Africa, south-eastern France and Italy have taken Bibliography place since the end of the Tertiary (Toumi & ABE, Y. 1988. Two host races in Andricus mukaigawae Lumaret, 1998). On the basis of this data, the (Mukaigawa) (Hymenoptera: Cynipidae). Appl. Ent. origin of A. hispanicus may be explained Zool., 23(4): 381-387. ABE, Y. 1991. Host race formation in the gall wasp through a host shift favoured by a closer Andricus mukaigawae. Entomol. Exp. Appl., 58: 15- proximity of Q. suber to Q. cerris than at pre- 20. sent and a subsequent geographical isolation ABE, Y. 1998. Karyotype differences and speciation in the gall wasp Andricus mukaigawae (s. lat.) caused by cold periods. The Iberian origin of (Hymenoptera: Cynipidae), with description of the Q. suber suggests that the origin of A. new species A. kashiwaphilus. Ent. Scand., 29: 131- 135. hispanicus probably lies in the Iberian ATKINSON, R. J. 2000. The genetic analysis of natu- Peninsula, and subsequent glaciations would ral history, reproductive strategy and population make the Iberian Peninsula and North Africa structure in European oak gallwasps (Hymenoptera: Cynipidae). PhD Thesis. University of Oxford. perfect refuges for this species. BEIJERINCK, M. W. 1902. Ueber die sexuelle Other species of Andricus may be similar Generation von Cynips kollari. Marcellia, 1: 13-18. cases to Andricus kollari sensu lato, since BELLIDO, D.; ROS-FARRÉ, P.; MELIKA, G & PUJADE-VILLAR, J. 2003. Review of the asexual their distributions include a great part of the forms of Andricus kollari species-group (Hymenoptera:

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