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Systematics of the Dioryctria Abietella Species Group (Lepidoptera: Pyralidae) Based on Mitochondrial DNA

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Systematics of the Dioryctria Abietella Species Group (Lepidoptera: Pyralidae) Based on Mitochondrial DNA SYSTEMATICS Systematics of the Dioryctria abietella Species Group (Lepidoptera: Pyralidae) Based on Mitochondrial DNA G. ROUX-MORABITO,1,2 N. E. GILLETTE,3 A. ROQUES,1 L. DORMONT,4 5 6 J. STEIN, AND F.A.H. SPERLING Ann. Entomol. Soc. Am. 101(5): 845Ð859 (2008) ABSTRACT Coneworms of the genus Dioryctria Zeller include several serious pests of conifer seeds that are notoriously difÞcult to distinguish as species. We surveyed mitochondrial DNA variation within the abietella species group by sequencing 451 bp of cytochrome oxidase subunit 1 (COI) and 572 bp of cytochrome oxidase subunit 2 (COII) genes from 64 individuals of six major species in the group. In addition to examining phylogenetic relationships within European members of the group, the study focused on the two most damaging species, D. abietivorella Grote from North America and D. abietella Denis & Schiffermu¨ ller from Europe and Asia, which have been considered taxonomically synonymous in the past. To detect different levels of divergence, we extensively sampled in seed orchards and natural forests for D. abietella on different hosts. Maximum parsimony and maximum likelihood analyses conÞrmed the monophyly of the abietella species group and its separation into three clades. The grouping of North American species (clade A) received strong support in both analyses, whereas relationships between clade A and the two European clades were weakly supported. Dioryctria simplicella Heinemann could not be unambiguously separated from D. abietella populations. The diverse haplotypes observed in the network analysis conducted with eight populations of polyphagous D. abietella suggested the presence of two distinct lineages in France. KEY WORDS Dioryctria, mitochondrial DNA, COI, COII, seed orchard The greater diversity of phytophagous insect clades merous examples of species complexes in which there compared with their nonphytophagous sister groups are evolutionarily signiÞcant entities that may or may has lead biologists to postulate that host plants strongly not represent species (Sperling 2003, Wahlberg et al. inßuence the diversiÞcation and speciation of herbiv- 2003). Because morphological characters of such re- orous insects (Kelley et al. 1999). Two patterns of lated species or subspecies are very hard to distin- association between phytophagous insects and their guish, their autecology and host plants are often used host plants exist, with some species using a diversity of for taxonomic identiÞcation, but the use of such labile host taxa (polyphagy), and others being restricted to characters raises doubts about the validity of the tax- one particular plant species (monophagy). According onomic status of these taxa. to numerous studies (Bush 1975, Mitter and Futuyma Coneworms of the genus Dioryctria Zeller comprise 1979, Diehl and Bush 1984, Tauber and Tauber 1989, several species groups within which numerous species Dres and Mallet 2002, Rundle and Nosil 2005), have been identiÞed mainly on the basis of their larval changes in host preference can be critical to the for- host plant, but also by forewing morphology and ge- mation of new species. Such genetic differentiation ography (Neunzig 2003). These coneworms are seri- has been associated with host use in several polyph- ous pests of conifer seed cones in the Holarctic region agous species, which frequently consist of locally spe- Ͼ cialized populations, races, or even sibling species (Turgeon et al. 1994), where 70 species have been complexes (Menken 1996). Lepidoptera include nu- recorded (Du et al. 2005, Roe et al. 2006). Most of them are associated with the Pinaceae, especially with Pinus L., Picea A. Dietrich, Abies Miller, Larix Miller, and 1 INRA, Centre dÕOrle´ans, Unite´ de Zoologie Forestie`re, BP20619 Ardon, 45166 Olivet cedx, France. Pseudotsuga Carrie`re species (Hedlin et al. 1980, 2 Corresponding author, e-mail: geraldine.roux-morabito@orleans. Roques 1983, Cibria´n-Tovar et al. 1986, Neunzig 1990, inra.fr. Turgeon and de Groot 1992), with a few being ob- 3 PaciÞc Southwest Research Station, USDAÐForest Service, Al- bany, CA 94710. served on Taxodiaceae (Merkel 1984). Because these 4 Centre dÕEcologie Fonctionnelle et Evolutive, CNRS UMR 5175, species may drastically limit crops of genetically su- 1919 Route de Mende, 34293 Montpellier Cedex 5, France. perior seeds in seed orchards, their biology has been 5 Forest Health Technology Enterprise Team, USDAÐForest Ser- studied extensively during the past 40 yr (Lyons 1957, vice, Morgantown, WV 26505. 6 Department of Biological Sciences, University of Alberta, Edm- Zocchi 1961, Neunzig et al. 1964, Charles and Roques onton, AB T6G 2E9, Canada. 1977, Grant et al. 1993, Millar et al. 2005). 0013-8746/08/0845Ð0859$04.00/0 ᭧ 2008 Entomological Society of America 846 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 5 However, a paucity of clear morphological charac- correct pest species diagnoses. Thus, it is important ters for separating Dioryctria taxa creates taxonomic to focus on clarifying the status of taxonomically uncertainties that hinder the analysis of their host intractable taxa like Dioryctria species groups, so relationships (Chatelain and Goyer 1980, Hedlin et al. that effective control measures can be tailored to 1980, Sopow et al. 1996). Using a combination of ex- each species. ternal characters and adult genitalia, Mutuura and In taxonomic groups where morphological identi- Munroe (1972) deÞned seven species groups but Þcation is difÞcult, molecular characters, particularly could not deÞnitively place all the studied species into mtDNA, can help in assessing species boundaries groups (Du et al. 2005). Among these groups, the (Sperling and Hickey 1994, Brower 1999, Caterino et abietella species group comprises 13 species and is al. 2000, Templeton 2001, Kerdelhue´ and Rasplus 2002, deÞned by the absence of raised scales on the forew- Hebert et al. 2003a, Wahlberg et al. 2003, Roe and ings, a feather-like maxillary palpus in the male, and a Sperling 2007b). Several properties make mtDNA a narrow valva in the male genitalia. According to Mu- good marker of species limits (Avise 1991, Sperling tuura and Munroe (1972, 1973) and Neunzig (2003), 2003, Wahlberg et al. 2003). It is a nonrecombining, this group includes the widespread Palaearctic spe- maternally inherited genome, with a smaller effective cies D. abietella Denis & Schiffermu¨ ller, and species population size that leads to shorter coalescence times from Europe (D. pineae Staudinger, D. mendacella (Moore 1995). Moreover, gene trees may be more Staudinger, D. simplicella Heinemann ϭ D. mutatella likely to reßect species trees when using mitochon- Fuchs, Fazekas 2002), North Africa (D. alloi Barbey, drial markers (Avise 2000, Sperling 2003). Thus, the D. peyerimhoffi Joannis), Asia (D. stenopterella Amsel, rapid evolution of mtDNA sequences has often been D. assamensis Mutuura, D. raoi Mutuura), North used in intraspeciÞc studies (Avise 2000) as well as in America (D. abietivorella Grote, D. ebeli Mutuura & investigating relationships of closely related species in Munroe, D. pinicolella Amsel), and Central America Lepidoptera (Bogdanowicz et al. 1993; Brower and (D. sysstratiotes Dyar). DeSalle 1994; Brower 1999; Brown et al. 1994; Sperling Dioryctria abietella and D. abietivorella are un- and Hickey 1994; Sperling et al. 1995; Landry et al. doubtedly the most important lepidopteran pests of 1999; Kruse and Sperling 2001; Sperling 2003; Wahl- conifer cones in Europe and North America (Roques berg et al. 2003; Du et al. 2005; Roe and Sperling 1983, Hedlin et al. 1980). They both have a wide host 2007a,b). So far, no molecular study has been per- range for larval development. So far, D. abietella has formed across the widespread and economically im- been recorded from Western Europe and Scandinavia portant European D. abietella coneworm group; and to the Russian Far East and northern China on a broad genetic and biochemical analyses of Dioryctria have so range of hosts, including cones of pine (Pinus spp.), far been primarily limited to North American and spruce (Picea spp.), larch (Larix spp.), Þr (Abies spp.), Chinese species (Richmond and Page 1995, Du et al. and Douglas-Þr [Pseudotsuga menziesii (Mirb.) 2005, Roe et al. 2006). Franko], and more rarely twigs, buds, and adelgid- Here, we review species delimitations and phylo- induced galls (Roques 1983). D. abietivorella has been genetic relationships within the Dioryctria abietella reported from Alaska to central Mexico, and from species group based on mtDNA sequences. We give California to Newfoundland, on Ͼ20 different hosts, special emphasis to the taxonomic status of the two including pine, spruce, and Douglas-Þr (Lyons 1957, most damaging Dioryctria species of this group, Hedlin et al. 1980, Turgeon and de Groot 1992). Be- namely, European D. abietella and North American D. cause these two species are generally similar in genital abietivorella. characters, they have variously been considered un- der the names D. abietella, D. assamensis, and D. raoi Materials and Methods (Munroe 1959, Byun et al. 1998). More recently, there has been similar confusion Coneworm Collections. A total of 67 specimens among European Dioryctria species such as D. abi- were selected for this study, 61 within the Dioryctria etella, D. simplicella, and even species outside the abietella species group (29 specimens identiÞed as D. abietella group such as D. schuetzeella Fuchs (Charles abietella, nine D. mendacella, two D. pineae, eight D. and
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