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Systematics of Pistacia: Insights from Specialist Parasitic Aphids

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Systematics of Pistacia: Insights from Specialist Parasitic Aphids Inbar • Aphids and Pistacia classification TAXON 57 (1) • February 2008: 238–242 Systematics of Pistacia: Insights from specialist parasitic aphids Moshe Inbar Department of Evolutionary & Environmental Biology, University of Haifa, Haifa 31905, Israel. [email protected] Clarifying the systematics of the genus Pistacia (Anacardiaceae) has been a challenging task. The use of sev- eral classical and modern classification tools resulted in disagreements. Pistacia spp. are the obligate hosts of highly specialized gall-forming aphids (Homoptera: Fordinae). It is well known that closely related species of insects may utilize closely related plants. A complete linkage cluster analysis of Pistacia species, based on presence/absence of thirteen aphid genera, is presented. Aphids recognized between evergreen and New World Pistacia species. Other Pistacia species are clustered into two groups: “Vera” (P. vera, P. atlantica, P. mutica) and “Khinjuk” (P. khinjuk, P. chinensis, P. integerrima, P. palaestina, P. terebinthus). Fordinae contribution to Pistacia taxonomy at the species and hybrid levels is discussed. The close association between insect herbivores and their hosts deserves to be used more often by plant taxonomists. KEYWORDS: aphids, cluster analysis, gall, Pistacia, taxonomy atlantica Desf.) and Terebinthus (P. chinensis Bunge, P. INTRODUCTION khinjuk Stocks, P. palaestina Bois., P. terebinthus L., P. vera L.). The latter section is composed of deciduous trees … aphids could probably be much more utilized with unwinged leaf rachis and sclerified drupes. Because in decision-making in systematic botany. of its winged leaf rachis, P. atlantica was placed in the (D. Hille Ris Lambers, 1979) separate Butmela section (Zohary, 1952). This early char- acterization by Zohary has been challenged by modern The pistachio tree, Pistacia vera L. (Anacardiaceae) molecular analyses. Parfitt & Badenes (1997) recognized was first cultivated in Central Asia (Iran, Afghanistan), two sections: “Lentiscus” (P. lentiscus L., P. mexicana then spread to the Middle East, and eventually to other Kunth, P. texana Swingle, P. weinmannifolia Poisson) parts of the world (Hormaza & al., 1994). The grow- and a monophyletic group (“Terebinthus”) composed of ing interest in pistachio cultivation stresses the need for all other species. Golan-Goldhirsh & al. (2004) placed vigorous rootstocks based on related wild Pistacia spe- P. atlantica in a separated, still questionable position. cies. Therefore, identification and conservation of wild Kafkas & Perl-Treves (2002) came out with two differ- Pistacia species and their hybrids have become highly ent subdivisions. One includes the big, single-trunk trees important, and germplasm collections have been estab- (P. atlantica, P. eurycarpa, P. integerrima, P. khinjuk, P. lished (Sheiban, 1995; Golan-Goldhirsh & Kostiukovsky, vera), and the other group is composed of the shrubs and 1998). Due to misnaming, polymorphism and the exis- small trees (P. lentiscus, P. mexicana, P. palaestina, P. tence of hybrids, the classification of the genus Pistacia texana, P. terebinthus). is not fully clear. Since the seminal monograph by Zohary Pistacia spp. are the obligate host for specialized (1952), several methods have been used to identify Pista- gall-forming aphids (Homoptera: Fordinae). Gall-form- cia species and construct their phylogenetic relationships. ing insects have very close relationships with their host The methods employed include morphological, anatomi- plants. The galling process involves intimate crosstalk cal, cytological, palynological, physiological and molecu- between the plant and the insect genotypes. The insects lar analyses (Zohary, 1952; Grundwag & Werker, 1976; are obligated to a specific host plant species, organ and Parfitt & Badenes, 1997; Kafkas & al., 2002; Katsiotis tissue (Weis & al., 1988). Indeed, several studies have & al., 2003; Golan-Goldhirsh & al. 2004; Ahmad & al., used gall-forming insects as a tool in plant systemat- 2005). But some confusion and disagreements on Pistacia ics (Meeuse, 1973; Aguilar & Boecklen, 1992; Floate classification still exist at all levels. & Whitham, 1995; Floate & al., 1996; Abrahamson & Based on morphological characters, Zohary (1952) al., 1998; Burckhardt & Basset, 2000). About thirty spe- divided the genus Pistacia into four sections: Lentiscella cies of gall-forming aphids belonging to the subfamily (New World species), Lentiscus (evergreens), Butmela (P. Fordinae (Pemphigidae) are associated with the genus 238 TAXON 57 (1) • February 2008: 238–242 Inbar • Aphids and Pistacia classification Pistacia (Blackman & Eastop, 1994). Most species are found in Central Asia and in Mediterranean-type habi- MATERIALS AND METHODS tats in Asia, Europe and North Africa (Bodenheimer & Aphids’ taxonomy might also be problematic due Swirski, 1957; Koach & Wool, 1977). The galls are highly to the wide distribution of aphids and plants, and the divergent in shape and size (Koach & Wool, 1977; Inbar morphological plasticity within species at different gen- & al., 2004). Usually each aphid species makes a specific erations and stages, which cause misidentifications, and gall on specific Pistacia species in which they feed on consequently misinterpretations. In order to eliminate the phloem sap (Inbar & Wool, 1995; Inbar & al., 1995). some of the confusion, this analysis was restricted to the The complex life cycle of the aphids includes sexual and more consensus genus level. The taxonomic literature was asexual reproduction and regular alternation between the thoroughly reviewed (see references in Table 1). Once primary Pistacia host and roots of non-specific second- the list of aphid genera was completed (literature review, ary hosts. The basic life cycle (which may have a few personal information), a cluster analysis was conducted modifications) is as follows: In early spring the galls are based on presence/absence of the aphid genera on each formed by the first instar nymphs (fundatrices) hatching Pistacia, using the complete linkage model with Pearson’s from overwintering eggs. Within each gall, two to three r distances of the Statistica software package (StatSoft Inc. additional aphid generations are produced parthenogeneti- Tulsa, OK, U.S.A.). cally. In fall winged aphids (fall migrants) disperse from the galls and the subsequent generations develop on the secondary hosts. The next spring, another winged morph (sexuparae) migrates back to the Pistacia and gives birth RESULTS AND DISCUSSION to the sexual stage (males and females). After mating, the Thirteen aphid genera were recognized in the current fertilized eggs remain on the tree, until the fundatrices analysis (Table 1). This list is slightly different from the hatch the following year (Bodenheimer & Swirski, 1957; one complied by Blackman & Eastop (1994). For example, Wool, 1984). they listed Smynthurodes betae from P. terebinthus, and The aim of this paper was to use the gall-forming the aphid genus Forda on P. lentiscus. According to the aphids as zoologically-based method for identifying spe- current survey and personal observations, these are most cies, inbreeds and relatedness among Pistacia species. probably mistakes. Blackman & Eastop (1994) also noted Table 1. List of gall-forming aphids (genera) and Pistacia hosts, recognized in this study. See text for discrepancies with Blackman & Eastop (1994). Aphid genus Pistacia species References Aloephagous aethiopica Blackman & Eastop, 1994 Aploneura lentiscus Koach & Wool, 1977 Asiphonella chinensis, khinjuk, palaestina Remaudière & Tao, 1957; Davatchi, 1958; Koach & Wool, 1977 Baizongia chinensis, integerrima, khinjuk, palaestina, Davatchi, 1958; Zhang, 1995; Chakrabarti, 1998; terebinthus Pérez Hidalgo & Nieto Nafría, 2003; Chaetogeoica chinensis Remaudière & Tao, 1957 Forda atlantica, chinensis, integerrima, khinjuk, mutica, Davatchi, 1958; Blackman & Eastop, 1994; Chakra- palaestina, terebinthus, vera barti, 1998; Pérez Hidalgo & Nieto Nafría, 2003 Fordini a atlantica Koach & Wool 1977; Wool & Manheim (pers comm.) Geoica atlantica, integerrima, khinjuk, mutica, palaestina, Davatchi 1958; Brown & Blackman 1994; terebinthus Chakrabarti 1998 Geopemohigus mexicana, texana Muñoz-Viveros & Remaudière, 1999 Paracletus khinjuk, palaestina, terebinthus Davatchi, 1958; Blackman & Eastop, 1994 Rectinasus khinjuk, palaestina Davatchi, 1958; Koach & Wool, 1977 Slavum atlantica, mutica, vera Davatchi, 1958; Koach & Wool, 1977 Smynthurodes atlantica, mutica Davatchi, 1958; Koach & Wool, 1977 Note: No galls are known from P. saporta. aAccording to D. Wool, O. Manheim (submitted MS) and G. Remaudière (pers. comm.) the Fordini spp. listed in Koach & Wool (1977) belong to a new genus. 239 Inbar • Aphids and Pistacia classification TAXON 57 (1) • February 2008: 238–242 that P. vera bears three aphid genera (Baizongia, Geoica, previous morphological and molecular analyses found Paracletus) that were not mentioned in the thorough study P. vera and P. khinjuk closely related (Zohary, 1952; of the Iranian fauna on Pistacia (Davatchi, 1958). Because Parfitt & Badenes, 1997; Kafkas & Perl-Treves, 2002; P. vera is cultivated and different studies might be in- Golan-Goldhirsh & al., 2004). Due to its wide distribu- fluenced by its variety, two sets of cluster analyses were tion, its tendency to form hybrids, and its local misnaming conducted: with and without the three above-mentioned (Browicz, 1988; Kafkas & Perl-Treves, 2002), some ento- genera on this tree. Nevertheless,
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