Russian Entomol. J. 20(3): 265–271 © RUSSIAN ENTOMOLOGICAL JOURNAL, 2011

Morphotypes of chromosome sets and pathways of karyotype evolution of parasitic

Ìîðôîëîãè÷åñêèå òèïû õðîìîñîìíûõ íàáîðîâ è íàïðàâëåíèÿ ýâîëþöèè êàðèîòèïà ïàðàçèòè÷åñêèõ ïåðåïîí÷àòîêðûëûõ (Hymenoptera)

V.E. Gokhman Â.Å. Ãîõìàí

Botanical Garden, Moscow State University, Moscow 119991, Russia. E-mail: [email protected] Áîòàíè÷åñêèé ñàä Ìîñêîâñêîãî ãîñóäàðñòâåííîãî óíèâåðñèòåòà, Ìîñêâà 119991, Ðîññèÿ.

KEY WORDS: chromosomes, karyotype evolution, morphotypes, parasitic Hymenoptera. ÊËÞ×ÅÂÛÅ ÑËÎÂÀ: õðîìîñîìû, ýâîëþöèÿ êàðèîòèïà, ìîðôîëîãè÷åñêèå òèïû, ïàðàçèòè÷åñêèå ïåðåïîí÷àòîêðûëûå.

ABSTRACT. Chromosomal diversity of parasitic ly [Imai et al., 1988; Hoshiba, Imai, 1993]. Fur- Hymenoptera has been analyzed with the help of the thermore, karyotypes, or rather karyomes (term intro- logical possibility space approach. Using three param- duced by Smirnov [1991]), usually evolve as holistic eters (haploid chromosome number, length ratios of objects [Lukhtanov, 1999] (see also Rasnitsyn, 1987), chromosomes within the haploid set, and the degree of and construction of the so-called chromosomal alter- karyotypic “metacentricity”), 18 classes, or morpho- ation networks [Imai, 1991, 1993], an apparent tool logical types, of chromosome sets have been delimited, proposed for analysis of karyotype evolution in many of which only 13 contain at least one karyotype. Possi- groups of living organisms including Hymenoptera, is ble major pathways of karyotypic transformation in probably unable to describe this process in an adequate parasitic have been outlined. manner. The main aim of the present paper is therefore a thorough analysis of the major morphotypes and path- ÐÅÇÞÌÅ. Õðîìîñîìíîå ðàçíîîáðàçèå ïàðàçè- ways of karyotypic transformation in parasitic Hy- òè÷åñêèõ Hymenoptera ïðîàíàëèçèðîâàíî ñ ïîìî- menoptera. ùüþ ïîäõîäà, ïðåäóñìàòðèâàþùåãî ñîçäàíèå ïðî- ñòðàíñòâà ëîãè÷åñêèõ âîçìîæíîñòåé. Ñ èñïîëüçî- Materaial and methods âàíèåì òðåõ ïàðàìåòðîâ (ãàïëîèäíîå ÷èñëî õðîìî- ñîì, ñîîòíîøåíèå äëèí õðîìîñîì â ãàïëîèäíîì To cover the whole range of karyotypic variation in íàáîðå è ñòåïåíü «ìåòàöåíòðè÷íîñòè» êàðèîòèïà) parasitic wasps, their chromosome sets have been ana- óñòàíîâëåíî 18 êëàññîâ (ìîðôîëîãè÷åñêèõ òèïîâ) lyzed by means of the technique that is widely used in õðîìîñîìíûõ íàáîðîâ, èç êîòîðûõ òîëüêî 13 âêëþ- evolutionary morphology, namely, by delimitation of ÷àþò õîòÿ áû îäèí êàðèîòèï. Îïðåäåëåíû îñíîâ- the so-called logical possibility space (see Meyen, íûå ïðåäïîëàãàåìûå íàïðàâëåíèÿ ïðåîáðàçîâàíèé 1975). To adequately describe it, three main parame- êàðèîòèïà ïàðàçèòè÷åñêèõ ïåðåïîí÷àòîêðûëûõ. ters have been selected to characterize more or less substantial groups of parasitic Hymenoptera: (a) hap- Introduction loid chromosome number (n = 3 to 7, 8 to 13 and 14 to 23); (b) length ratios of chromosomes within the hap- Parasitic Hymenoptera belong to the very large, loid set (one or two chromosomes are not less than 1.5 taxonomically complicated and economically impor- times shorter/longer than the others, or they more or tant group of [Rasnitsyn, 1980]. Nevertheless, less gradually decrease in size; if chromosomes are the detailed picture of karyotype evolution of parasitic obviously uneven by size in any other way, those kary- wasps is far from being complete, although a few suc- otypes are conditionally included into the latter class); cessful attempts of its reconstruction have been made (c) degree of karyotypic “metacentricity” [not less than (see Gokhman, 2009). Moreover, research of that kind one-half of all chromosomes are metacentric in a broad usually requires a detailed chromosomal study of a sense (including submetacentrics), or acrocentrics (again certain group, but comparatively few karyotypes of in a broad sense, including subtelocentrics) predomi- parasitic Hymenoptera have been studied to that extent nate within the given karyotype]. Karyotypic data from up to now, apart from aculeate Hymenoptera, especial- Gokhman [2009] and a number of recent papers [Gokh- 266 V.E. Gokhman man, Gumovsky, 2009; Gokhman, 2010b; Gokhman et doidea: many species of the families , Tri- al., 2010] together with a few unpublished observa- chogrammatidae and some other groups. tions made by the author were used in the analysis; (8) : : a few Pim- however, information on chromosome sets of certain pliformes, most Ichneumoniformes and a number of groups was also taken from a few extra papers [Drey- Ophioniformes; : species of the genus Bas- fus, Breuer, 1944; Hung, 1982; Sanderson, 1988; Hoshi- sus Fabricius, 1804 (Agathidinae) and a few other ba, Imai, 1993; Abe, 1998; Baldanza et al., 1999; Fusu, groups. Diaprioidea: : all karyotypically 2008]. Using this technique, I have focused on rear- known species. : Cynipidae: species of the rangements that cause substantial changes between cer- genus Diplolepis Geoffroy, 1762; : a few spe- tain types of chromosome sets of parasitic wasps. “With- cies. : Scelionidae: Telenomus fariai in-type” rearrangements are therefore not considered Costa Lima, 1927. : : Den- in the present paper, although they may well be respon- drocerus carpenteri (Curtis, 1829). Chalcidoidea: My- sible for additional karyotypic diversity (see for details maridae: Anaphes iole Girault, 1911; : a Gokhman, 2009). The diversity of morphotypes of chro- few species; : a few species; : mosome sets within all karyotypically studied super- Elachertus sp. families of parasitic Hymenoptera has been analyzed (9) : : Gasteruption jacu- using corresponding phylogenetic reconstructions (taken lator (Linnaeus, 1758). Ichneumonoidea: Ichneu- from Gokhman [2009] and a few other sources) to monidae: most Pimpliformes and a few Ichneumoni- reveal main transformation pathways of karyotype evo- formes; Braconidae: a number of species mostly be- lution in the group studied. The principal phylogeny of longing to the cyclostome group of subfamilies (Do- the parasitic Hymenoptera used in the present paper is ryctinae, Opiinae, Alysiinae etc.). based on the study by Ronquist et al. [1999], which, in (10) No parasitic wasps having chromosome sets of turn, is a computerized reanalysis of the dataset pre- that kind are currently known. sented in the pioneering work by Rasnitsyn [1988]. In (11) Ichneumonoidea: Ichneumonidae: many Ophio- the end, possible mechanisms of the above mentioned niformes and a few Ichneumoniformes; Braconidae: a transformations have been suggested. few species, e.g. Alysia manducator (Panzer, 1799) (Alysiinae). Cynipoidea: Cynipidae: most species. Chal- Results and discussion cidoidea: : a number of species; Eurytomi- dae: a number of species; Aphelinidae: some species of Morphotypes of chromosome sets of parasitic the subfamily Coccophaginae. Hymenoptera (12) Ichneumonoidea: Ichneumonidae: a few Pim- Eighteen possible classes (morphological types) of pliformes (Orthocentrinae) and Ichneumoniformes chromosome sets of parasitic wasps have been delimit- (Cryptinae and Ichneumoninae). ed. General distribution of those morphotypes by su- (13) Chalcidoidea: Aphelinidae: a few species of perfamily is listed in the Table. This information is the genera Encarsia Förster, 1878 and Aphelinus Dal- also given below in more detail. man, 1820. (1) Ichneumonoidea: Ichneumonidae: Ophioni- (14) Ichneumonoidea: Ichneumonidae: a few Ophio- formes (Mesochorinae): Mesochorus sp.; Braconidae: niformes and Ichneumoniformes (Ichneumoninae). Aphidius matricariae Haliday, 1834 (Aphidiinae) and (15) No parasitic wasps having karyotypes of that most Cheloninae. Cynipoidea: Cynipidae: Andricus kind are currently known. mukaigawae (Mukaigawa, 1913). Chalcidoidea: many (16) Chalcidoidea: Aphelinidae: Encarsia tricolor species of the families Eulophidae, , Eu- Förster, 1878; : Eupelmus linearis Förster, pelmidae and some other groups. 1860. (2) Ichneumonoidea: Ichneumonidae: Ichneumoni- (17) Ichneumonoidea: Ichneumonidae: Ichneumon- formes (Ichneumoninae): Dirophanes fulvitarsis (Wes- iformes: a few Ichneumoninae. Cynipoidea: Figitidae: mael, 1845) and Vulgichneumon saturatorius (Linnae- Ganaspis xanthopoda (Ashmead, 1896) and Leptopili- us, 1758); Braconidae (Meteorinae): Meteorus versi- na boulardi (Barbotin, Carton et Kellner-Pillault, 1979). color (Wesmael, 1835). Chalcidoidea: Mymaridae: Ana- Chalcidoidea: Eupelmidae: Arachnophaga picardi (Ber- phes listronoti Huber, 1997. nard, 1936); Encyrtidae: Ageniaspis fuscicollis (Dal- (3) Ichneumonoidea: Ichneumonidae: Ichneumoni- man, 1820). formes (Ichneumoninae): Virgichneumon digrammus (18) Evanioidea: Gasteruptiidae: Gasteruption as- (Gravenhorst, 1820). sectator (Linnaeus, 1758). Ichneumonoidea: Ichneu- (4) – (6). No parasitic wasps having karyotypes of monidae: Ophioniformes (Orthopelmatinae): Orthopel- that kind are currently known. ma mediator (Thunberg, 1824). (7) Ichneumonoidea: Ichneumonidae: Ophioni- formes (Tryphoninae): Netelia latungula (Thomson, Main pathways of karyotype evolution of para- 1888); Braconidae: Charmon cruentatus Haliday, 1833 sitic Hymenoptera (Charmontinae) and a few Aphidiinae. Cynipoidea: It is difficult at present to precisely identify the Cynipidae: Andricus kashiwaphilus Abe, 1998. Chalci- ancestral karyotype for the parasitic Hymenoptera. Spe- Morphotypes of chromosome sets and karyotype evolution of parasitic Hymenoptera 267

Table. Distribution of the morphological types of chromosome sets of parasitic wasps by superfamilies. Òàáëèöà. Ðàñïðåäåëåíèå ìîðôîëîãè÷åñêèõ òèïîâ õðîìîñîìíûõ íàáîðîâ ïàðàçèòè÷åñêèõ ïåðåïîí÷àòîêðûëûõ ïî íàäñåìåéñòâàì.

Size differentiation M:A Haploid chromosome number (n) of chromosomes 3–7 8–13 14–23 One or two ³1 (1) (2) (3) chromosomes Ichneumonoidea-5 Ichneumonoidea-3 Ichneumonoidea-1 shorter than the Cynipoidea-1 Chalcidoidea-1 others Chalcidoidea-31 <1 (4) (5) (6) All chromosomes ³ 1 (7) (8) (9) more or less Ichneumonoidea-6 Ichneumonoidea-64 Evanioidea-1 gradually decrease Cynipoidea-1 Diaprioidea-2 Ichneumonoidea-18 in size Chalcidoidea-34 Cynipoidea-5 Platygastroidea-1 Ceraphronoidea-1 Chalcidoidea-6 <1 (10) (11) (12) Ichneumonoidea-10 Ichneumonoidea-10 Cynipoidea-6 Chalcidoidea-12 One or two ³ 1 (13) (14) (15) chromosomes Chalcidoidea-5 Ichneumonoidea-4 longer than the <1 (16) (17) (18) others Chalcidoidea-2 Ichneumonoidea-2 Evanioidea-1 Cynipoidea-2 Ichneumonoidea-1 Chalcidoidea-2

Remarks. M : A — ratio of metacentrics (M) to acrocentrics (A) in a given chromosome set. Amounts of karyotypically studied species with certain morphotypes of chromosome sets are given for every superfamily. Ïðèìå÷àíèÿ. M : A — ñîîòíîøåíèå ìåòàöåíòðèêîâ (M) è àêðîöåíòðèêîâ (A) â òîì èëè èíîì õðîìîñîìíîì íàáîðå. Êîëè÷åñòâî êàðèîëîãè÷åñêè èçó÷åííûõ âèäîâ ñ äàííûì ìîðôîëîãè÷åñêèì òèïîì õðîìîñîìíûõ íàáîðîâ äàíî äëÿ êàæäîãî íàäñåìåéñòâà. cifically, in the superfamily Evanioidea that is consid- trics could prevail in this chromosome set (i.e. it could ered the most basal superfamily of parasitic wasps with refer to morphotype (9) [Gokhman, 2009]). studied chromosome sets (Fig. 1, see also Fig. 5.5 in Morphological types of chromosome sets of the [Gokhman, 2009]), karyotypes of only two species of superfamily Ichneumonoidea are very diverse, and the genus Gasteruption Latreille, 1776 (Gasterupti- therefore the reconstruction of karyotype evolution of idae) have been examined. In Gasteruption jaculator, this group that is given below should be considered as n = 16, the ratio of metacentrics to acrocentrics is provisional. Specifically, eleven morphotypes have been roughly 1:1, and all chromosomes more or less gradu- found in the families Ichneumonidae and Braconidae. ally decrease in size. However, in G. assectator n = 14 Among those, morphological types (9) and (12), i.e. and most chromosomes are acrocentric, although two karyotypes with n = 14 and more, predominate in less metacentric chromosomes are substantially longer than advanced groups of the above mentioned families, i.e. the others. The latter karyotypic feature probably indi- in the Pimpliformes and Ichneumoniformes (Ichneu- cates two chromosomal fusions that have occurred in monidae) as well as in the cyclostome group of fami- the karyotype of G. assectator, and therefore the an- lies (Braconidae). At present, I would suggest that the cestral chromosome set of the Evanioidea (and proba- ancestral karyotype, at least for the Ichneumonidae, is bly of the parasitic Hymenoptera in general) could (12). This morphotype is retained in a few Orthocentri- have the n value about 16 and a substantial proportion nae (Pimpliformes), Cryptinae and Ichneumoninae (Ich- of acrocentrics. Moreover, if chromosome sets of puta- neumoniformes), although many other species of those tive ancestral groups within the suborder Symphyta are groups as well as most cyclostome Braconidae have concerned [Westendorff, 2006; Gokhman, 2010c], high- metacentric-rich karyotypes, i.e. those of morphologi- er chromosome numbers in this group are usually asso- cal type (9). In addition to the above mentioned trans- ciated with higher proportions of acrocentric chromo- formation from (12) to (9), further transition from (9) somes (e.g. in the Xyeloidea, Pamphilioidea and cer- to (8) can be observed in the tribe Polysphinctini (Pim- tain ), and therefore the ancestral karyotype plinae) with n = 8–13. In the Ichneumoniformes, a of parasitic Hymenoptera might well have this feature, similar change has probably resulted in the origin of i.e. its morphological type can be classified as (12), chromosome sets of certain Cryptinae, e.g. Aptesis although I have previously hypothesized that metacen- gravipes (Gravenhorst, 1829), and most Ichneumoni- 268 V.E. Gokhman

Fig. 1. Evolutionary transformations of morphological types of chromosome sets within various superfamilies of parasitic Hy- menoptera. Reconstructed ancestral morphotypes are given in brackets. Plain arrows indicate transformations that are unique at the superfamily level, thick arrows indicate independent multiple transformations, and dashed arrows indicate possible alternative pathways of karyotype evolution. Ðèñ. 1. Ýâîëþöèîííûå ïðåîáðàçîâàíèÿ ìîðôîëîãè÷åñêèõ òèïîâ õðîìîñîìíûõ íàáîðîâ â ïðåäåëàõ ðàçëè÷íûõ íàäñåìåéñòâ ïàðàçèòè÷åñêèõ Hymenoptera. Ðåêîíñòðóèðîâàííûå ïðåäêîâûå ìîðôîëîãè÷åñêèå òèïû ïðèâåäåíû â êâàäðàòíûõ ñêîáêàõ. Îáû÷- íûå ñòðåëêè îáîçíà÷àþò ïðåîáðàçîâàíèÿ, óíèêàëüíûå íà óðîâíå íàäñåìåéñòâà, óòîëùåííûå ñòðåëêè — íåçàâèñèìûå íåîäíîêðàò- íûå ïðåîáðàçîâàíèÿ, à ïóíêòèðíûå ñòðåëêè — âîçìîæíûå àëüòåðíàòèâíûå ïóòè ýâîëþöèè êàðèîòèïà. Morphotypes of chromosome sets and karyotype evolution of parasitic Hymenoptera 269 nae. Moreover, a transition from (12) to (11) is sup- chromosome sets of the Cynipidae, morphotype (11) posed to form the karyotype of Mesostenus gracilis could be considered as an ancestral one for the whole Cresson, 1864 (Cryptinae). In the Ichneumoninae, one superfamily. Chromosome sets of morphological types of the above mentioned morphotypes, i.e. (8), is be- (8), (1), (7) and (17) are therefore derived from the lieved to be an ancestral one for the subfamily. From ancestral character state. this starting point, a number of transitions took place Chromosomal morphology of the only species of [to (2) in Dirophanes fulvitarsis and Vulgichneumon the superfamily Platygastroidea, namely, Telenomus saturatorius and further to (3) in Virgichneumon di- fariai (Scelionidae) has been studied up to now [Drey- grammus; to (9) in Chasmias motatorius (Fabricius, fus, Breuer, 1944]. According to these results, its kary- 1775); to (11) in certain species of the subtribe Crat- otype formally belongs to morphological type (8). How- ichneumonina; to (14) in Eurylabus torvus Wesmael, ever, a considerable proportion of acrocentrics within 1845 and to (17) in Cratichneumon fabricator (Fabri- the chromosome set may well indicate that the real cius, 1793)]. In the Ophioniformes, the only studied ancestral karyotype for the superfamily could belong to species of Orthopelma Taschenberg, 1875 (the basal morphotype (11). Although the possibility that the above genus that is sometimes included in its own group, mentioned karyotype could be metacentric-rich cannot Orthopelmatiformes) has the chromosome set of mor- be excluded at present, the proposed hypothesis seems photype (18). This might indicate that the ancestral more plausible, especially if compared to ancestral karyotype of the Ophioniformes is also of morphologi- character states that are suggested for the Cynipoidea cal type (12), and the chromosome set of Orthopelma and Chalcidoidea (see below). has originated from the previous one through centric The only karyotypically studied species of the su- fusions. Many other Ophioniformes have karyotypes perfamily Ceraphronoidea, Dendrocerus carpenteri with decreased chromosome numbers, i.e. those of mor- (Megaspilidae), demonstrates the chromosome set of photype (11) and sometimes (8); the latter chromo- morphotype (8). Analogously to the Platygastroidea, some sets seem to be derived in this particular case. however, the ancestral character state in the superfami- Moreover, process of pairwise centric fusions of the ly is suggested to be (11). former chromosome sets could result in the origin of In the superfamily Chalcidoidea, the family My- metacentric-rich, low-numbered karyotypes in this maridae is considered the most basal group (see e.g. group. For example, Hyposoter sp. (Campopleginae) [Gokhman, Gumovsky, 2009]). However, karyotypes has a diploid chromosome set of twelve pairs of acro- of only two species of the genus Anaphes Haliday, centrics that very gradually decrease in size. On the 1833 have been studied up to now within the whole contrary, chromosome number is twice less in Netelia family. Metacentrics prevail in both species, but the latungula [morphotype (7)] with six pairs of large meta- genus itself is far from being basal within Mymaridae centrics, thus suggesting the origin of the latter karyo- [Gokhman, Gumovsky, 2009], and therefore the ratio type by pairwise centric fusions. Chromosome sets of of metacentrics to acrocentrics will probably differ in Campoplex sp. [morphotype (14)] and Mesochorus sp. other Mymaridae. In addition, acrocentrics predomi- [morphotype (1)] are also likely to have similar ori- nate in a number of less advanced groups of the fami- gins, although at least some of them might represent lies Aphelinidae (subfamily Coccophaginae), Euryto- intermediate stages of the above mentioned process. midae and Encyrtidae, and therefore the chromosome Patterns of karyotype evolution in the family Braconidae set of morphotype (11) is considered as an ancestral are probably analogous to those of the Ichneumonidae. one for the superfamily. Several morphological types In the former group, there is also a clear trend towards of chromosome sets are likely to have originated from the emergence of specialized chromosome sets of mor- the latter one. Specifically, certain Aphelinidae, e.g. photypes (7) (e.g. in Charmon cruentatus) and (1) (e.g. Coccophagus lycimnia (Walker, 1839) and Eurytomi- in most Cheloninae) from less advanced ones, i.e. (8), dae, e.g. Sycophila biguttata (Swederus, 1795) have (9), and (11), although it is impossible at present to karyotypes of morphological type (8). Some other Aph- reconstruct the above mentioned patterns in detail. elinidae, however, have metacentric-rich chromosome In the superfamily Diaprioidea, only a few species sets with one or two chromosomes that are substantial- of the family Diapriidae have been studied. Karyotypes ly longer than the others, i.e. of morphological type of all parasitic wasps of this group can be classified (13). Moreover, karyotype of Encarsia tricolor that within morphological type (8), including Ismarus flav- also belongs to the Aphelinidae, together with Eupel- icornis (Thomson, 1859) that belongs to the genus mus linearis (Eupelmidae), differs from previous ones which is generally considered as relatively basal within by being acrocentric-rich, i.e. it falls into morphologi- the family. cal type (16). Chromosome sets of another morpho- Chromosome sets that belong to morphological types type, (17), have been found in Ageniaspis fuscicollis (8) and (11) prevail in the superfamily Cynipoidea. (Encyrtidae) as well as in Arachnophaga picardi (Eu- However, according to the phylogenetic reconstruction pelmidae). In addition, many species of the family provided by Ronquist [1999], the family Cynipidae is Eulophidae as well as Torymidae together with a few the most basal group with known karyotypes within the related families, certain Eupelmidae and Eurytoma ser- Cynipoidea. Since acrocentrics predominate within ratulae (Fabricius, 1798) (Eurytomidae) have karyo- 270 V.E. Gokhman types of morphological type (1). Finally, morphotype the end, low-numbered metacentric-rich chromosome (7) predominates in many “low-numbered” groups of sets of morphotype (7) mark final stages of the process chalcid wasps (e.g. and Chalcididae), al- of pairwise chromosomal fusions. The latter morpho- though it also occurs in a few species of the so-called logical type can be found within the Ichneumonoidea, “high-numbered” families, e.g. in Eurytoma compres- Cynipoidea and Chalcidoidea, although it is certainly sa (Fabricius, 1794) (Eurytomidae) and Metaphycus more widespread among chalcid wasps. stanleyi Compere, 1940 (Encyrtidae). The present study also reveals the previously un- It is also interesting to discuss possible reasons for derestimated role of centric fusions in karyotype evo- absence of certain morphotypes of chromosome sets. lution of parasitic wasps. This situation can probably For example, karyotypes with lower chromosome num- be explained by the fact that many events of that kind bers and the prevalence of acrocentrics that gradually have taken place in the superfamily Chalcidoidea, and decrease in size are unknown in parasitic wasps. This a number of groups of chalcid wasps (especially those pattern could be explained by the fact that acrocentric with less derived karyotypes, e.g. certain Eurytomidae chromosomes are prone to Robertsonian fusions that and Encyrtidae) were not enough karyotypically stud- result in appearance of large biarmed elements within ied until recently. low-numbered karyotypes. In turn, very short chromo- somes can be detected only within the latter chromo- ACKNOWLEDGEMENT. The present study was some sets with the prevalence of metacentrics, proba- partly supported by a research grant no. 10-04-01521 bly also because smaller acrocentrics could easily un- from the Russian Foundation for Basic Research. dergo centric fusions with the larger ones. On the con- trary, longer chromosomes can be found in a few high- References numbered karyotypes only if they are acrocentric-rich because this situation probably reflects initial stages of Abe Y. 1998. Karyotype differences and speciation in the gall the process of consecutive chromosomal fusions (see Andricus mukaigawae (s. lat.) (Hymenoptera: Cynipidae), with below). description of the new species A. kashiwaphilus // Entomolo- Since there are quite a few detailed studies of kary- gica scandinavica. Vol.29. P.131–135. Baldanza F., Gaudio L., Viggiani G. 1999. 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