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Two Species Within Dendroctonus Frontalis (Coleoptera: Curculionidae

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Two Species Within Dendroctonus Frontalis (Coleoptera: Curculionidae Two Species within Dendroctonus frontalis (Coleoptera: Curculionidae): Evidence from Morphological, Karyological, Molecular, and Crossing Studies Author(s): Francisco Armendáriz-Toledano, Alicia Niño, Brian T. Sullivan, Jorge Macías-Sámano, Javier Víctor, Stephen R. Clarke, and Gerardo Zúñiga Source: Annals of the Entomological Society of America, 107(1):11-27. 2014. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/AN13047 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. SYSTEMATICS Two Species Within Dendroctonus frontalis (Coleoptera: Curculionidae): Evidence From Morphological, Karyological, Molecular, and Crossing Studies FRANCISCO ARMENDA´ RIZ-TOLEDANO,1 ALICIA NIN˜ O,2 BRIAN T. SULLIVAN,3 2,4 1 5 1,6 JORGE MACI´AS-SA´ MANO, JAVIER VI´CTOR, STEPHEN R. CLARKE, AND GERARDO ZU´ N˜ IGA Ann. Entomol. Soc. Am. 107(1): 11Ð27 (2014); DOI: http://dx.doi.org/10.1603/AN13047 ABSTRACT Dendroctonus frontalis Zimmermann is considered one of the most important economic and ecological forest pests in the United States, Mexico, and Central America. Recently, two apparent morphological variants of this species were discovered occurring syntopically in Central America and southern Mexico. Morphotype A beetles lack a series of Þne parallel ridges on the episternal area of the prothorax that are present on morphotype B. The goal of the present work was to clarify the taxonomic status of the morphotypes of the D. frontalis species complex. Geometric morphometric analyses of seminal rod and spermatheca shape together with the characterization of 16 attributes of external morphology revealed differences in quantitative and qualitative characters that distinguished adults of the two morphotypes from each other as well as from the closely related species Dendroctonus vitei Wood and Dendroctonus mexicanus Hopkins. Karyotype analysis of morphotype B revealed a chromosomal formula (5AA ϩ Xyp) distinct from that found in morphotype A previously reported for D. frontalis (7AA ϩ Xyp). In the laboratory, forced intermorphotype crosses produced F1 progeny but at lower frequency than intramorphotype pairings, and dissections of spermatheca revealed a lower frequency of insemination at least one type of heterotypic cross. Phylogenetic analysis of the D. frontalis species complex based on 786 bp of the cytochrome oxidase I gene indicated that morphotypes B and A are two independent groups with 98% nodal support within D. frontalis. These data provide compelling evidence that the two syntopic morphotypes represent two distinct sibling species. KEY WORDS seminal rod, spermatheca, geometric morphometry, syntopic species, integrative taxonomy The genus Dendroctonus Erichson (Curculionidae: mis LeConte, Dendroctonus frontalis Zimmermann, Scolytinae) is widely distributed in North and Central Dendroctonus mexicanus Hopkins, and Dendroctonus America and Eurasia. They colonize and kill trees of vitei Wood (Lanier et al. 1988). The composition of the genera Larix Mill., Picea A. Dietr., Pseudotsuga the D. frontalis complex has changed virtually with Carrie`re, and Pinus L. (Wood 1982). Dendroctonus is almost every taxonomic review (Lanier et al. 1988), composed of 19 species, one of them with two sub- and species assignation has been based largely on species, which are ordered into different groups external morphological features (e.g., setal vestiture (Wood 1963, 1982; Lanier 1981; Kelley and Farrell and sculpturing of the elytral declivity, frons sculp- 1998; Zu´ n˜ iga et al. 2002a). The Dendroctonus frontalis ture, shape of epistomal process, and pronotal size and complex (sensu lato) is composed of the Pinus-infest- sculpture. Nevertheless, routine identiÞcation of the ing species Dendroctonus adjunctus Blandford, Den- more difÞcult species in the D. frontalis complex (e.g., droctonus approximatus Dietz, Dendroctonus brevico- D. frontalis, D. mexicanus, and D. vitei) cannot be performed with external morphological features 1 Instituto Polite´cnico Nacional, Escuela Nacional de Ciencias Bi- alone, because broad intraspeciÞc morphological vari- olo´gicas, Prol. de Carpio y Plan de Ayala, Col. Santo Tomas Del. Miguel Hidalgo, Me´xico D.F., CP 11340. ation exists, and key external character states can be 2 El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo distinguished only with practice. In contrast, seminal Aeropuerto km 2.5, Tapachula, Chiapas, Me´xico, CP 30700. rod shape and chromosome number have been shown 3 USDA Forest Service, Southern Research Station, 2500 Shreve- port Hwy., Pineville, LA 71360. to be reliable features for distinguishing these species 4 Current Address: Synergy Semiochemicals Corporation, 7061 (Vite´ et al. 1975; Lanier 1981; Wood 1982; Lanier et al. Meritt Ave., Burnaby, British Columbia, Canada, V5J 4R7. 1988; Zu´ n˜ iga et al. 2002a,b). With the exception of D. 5 USDA Forest Service, Forest Health Protection, 2221 N Raguet Lufkin, TX. vitei, species in the D. frontalis complex have been 6 Corresponding author, e-mail: [email protected]. characterized by karyological studies (Lanier 1981; 0013-8746/14/0011Ð0027$04.00/0 ᭧ 2014 Entomological Society of America 12 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 107, no. 1 Fig. 1. Analyzed anatomical structures of D. frontalis in both MA, morphotype A, and MB, morphotype B. Sculpture of preepisternal area: (a) MA smooth, (b) MB striated; rows of squamiform plates on eighth tergite: (c) MA, (d) MB; acute projections on posterior edge on squamiform plates in the median proximal area of the eighth tergite: (e) MA short and uniform, (f) MB variable in size; spermatheca: (g) MA with round cornu, aggregated striae on the nodulus, and Ϸ1/4 of body covered by striations, (h) MB with oval cornu, separated striae on the nodulus, and Ϸ1/2 of body covered by striations; seminal January 2014 ARMENDA´ RIZ-TOLEDANO ET AL.: EVALUATION OF MORPHS IN D. frontalis 13 Lanier et al. 1988; Zu´ n˜ iga et al. 2002a,b) as well as 10% KOH. After incubation, structures were im- mtDNA sequences (Kelley and Farrell 1998). mersed in 20% acetic acid solution to neutralize the Within the frontalis complex, D. frontalis (southern KOH and subsequently rinsed with 100% ethanol. The pine beetle) is an important economic and ecological genitalia were then dissected. For females, the eighth forest pest within its extensive geographic range, tergite and spermatheca from the same individual which includes the southeastern United States, Ari- were mounted on the same slide. For males, the sem- zona, Mexico, and Central America (Clarke and inal rod was separated from the genital capsule and all Nowak 2009). During periodic outbreaks, D. frontalis parts were mounted on the same slide. All structures are capable of overcoming the defenses of healthy were mounted in HoyerÕs medium on semipermanent pine trees and deforesting patches of the landscape slides for easy manipulation throughout the study. ranging in size from small “spots” to thousands of acres Character Analysis for the Two Morphs. Based on (Billings 2011). the presence or absence of striations on the preepis- Recently, two morphologically distinct variants of ternal area of the prothorax of 389 D. frontalis insects D. frontalis were identiÞed in collections from Central (Midtgaard and Thunes 2002; Sullivan et al. 2012, Fig. America and southern Mexico. Morphotype A (MA) 1; this paper Fig. 1a and b), we identiÞed 268 speci- beetles were on average somewhat smaller than mor- mens striaeless (MA) and 121 with striae (MB). These photype B (MB) beetles, and MA insects of both sexes insects were exhaustively examined to identify addi- lacked of a Þne series of ridges present in the preep- tional morphological characters for the correct isternal area of the prothorax morphotype MB beetles morphs identiÞcation. From 30 reviewed attributes, 16 (Midtgaard and Thunes 2002; Sullivan et al. 2012, Fig. were taxonomic characters potentially useful for mor- 1; this paper Fig. 1a and b). Although this last character photype separation: 10 were on the external cuticle (8 has been used to separate these morphs, a formal quantitative and 2 qualitative) and the rest were ter- analysis has not been conduced to evaluate its utility minaliaÕs characters (in the eighth tergite, sper- as taxonomic character. The morphotypes have been matheca, and seminal rod). found to differ signiÞcantly in production of known Adults beetles were examined at magniÞcations up Dendroctonus pheromone components (specimens to 90ϫ and were photographed with an Environmen- from Chiapas, Mexico) and in the composition of their tal Scanning Electron Microscope ESEM (Evo 40
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