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Genetic Structure of Graphocephala Atropunctata

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Genetic Structure of Graphocephala Atropunctata Genetic Structure of Graphocephala atropunctata (Hemiptera: Cicadellidae) Populations Across Its Natural Range in California Reveals Isolation by Distance Author(s): E. S. Ballman, P. F. Rugman-Jones, R. Stouthamer, and M. S. Hoddle Source: Journal of Economic Entomology, 104(1):279-287. 2011. Published By: Entomological Society of America DOI: 10.1603/EC10112 URL: http://www.bioone.org/doi/full/10.1603/EC10112 BioOne (www.bioone.org) is an electronic aggregator of bioscience research content, and the online home to over 160 journals and books published by not-for-profit 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. MOLECULAR ENTOMOLOGY Genetic Structure of Graphocephala atropunctata (Hemiptera: Cicadellidae) Populations Across Its Natural Range in California Reveals Isolation by Distance 1 1,2 1,2 1,2,3 E. S. BALLMAN, P. F. RUGMAN-JONES, R. STOUTHAMER, AND M. S. HODDLE J. Econ. Entomol. 104(1): 279Ð287 (2011); DOI: 10.1603/EC10112 ABSTRACT The genetic structure of 23 populations of Graphocephala atropunctata (Signoret) (Hemiptera: Cicadellidae: Cicadellinae), a vector of the plant pathogenic bacterium Xylella fastidiosa Wells et al., was investigated using ribosomal 28S and mitochondrial cytochrome C oxidase I gene sequences. The 28S sequences were identical across all G. atropunctata specimens and populations, but 16 mitochondrial haplotypes were detected and signiÞcant interpopulation differences were found F in the distribution of these haplotypes. Pairwise estimates of st correlated positively with geographical distance between populations, a phenomenon known as genetic isolation by distance. Thus, despite potential for widespread movement of G. atropunctata through nursery and agricultural industries, isolated populations of G. atropunctata have remained genetically distinct, suggesting that negligible numbers of G. atropunctata are actually transported or population interbreeding rarely occurs. The phylogenetic relationship between G. atropunctata and two additional congeners, Graphocephala cythura Baker and Graphocephala flavovittata Metcalf, which have overlapping distributions with G. atropunctata, also was investigated. Although 28S sequences of G. flavovittata were strikingly similar to those of G. atropunctata, mitochondrial DNA (mtDNA) suggests that both species are genetically distinct from G. atropunctata. KEY WORDS Graphocephala flavovittata, Graphocephala cythura, sharpshooters, cytochrome C oxidase I, 28S The blue-green sharpshooter, Graphocephala at- 2000) with the assumption that results apply to all ropunctata (Signoret) (Hemiptera: Cicadellidae: Ci- populations found throughout California. However, cadellinae), is a xylem-feeding leafhopper that vectors G. atropunctata occupies a northÐsouth latitudinal the bacterium Xylella fastidiosa Wells et al., the caus- range of Ϸ1,000 km across California and has limited ative agent of PierceÕs disease in grape (Vitis spp.) natural dispersal abilities (Severin 1949). Thus, op- vines. G. atropunctata is native to the western United portunities for interbreeding to occur between highly States, with a range that extends as far south as Nic- isolated populations across this vast range may be G. at- aragua in Central America (McKamey 2007). restricted, resulting in limited gene ßow and the de- ropunctata is common throughout California, and al- velopment of signiÞcant differences in reproductive though it is found primarily on wild grape and Rubus behavior, biology, and ecology between isolated pop- blackberry ( spp.), in humid riparian areas, it ulations. also feeds on a wide variety of native and exotic plants One readily observable difference between widely (Severin 1949). Polyphagy, wide distribution, and disparate populations of G. atropunctata is their mor- transmission of X. fastidiosa combine to make G. at- phology, in particular their color, which varies dra- ropunctata a perennial threat to the California grape matically from northern to southern California (Fig. industry, especially in the Napa Valley area of north- G. atropunctata ern California, where it is the primary vector of 1). Typically, from northern California PierceÕs disease (Purcell 1976). are dark green with faint markings on the body, Much of the research conducted on G. atropunctata whereas southern California populations are bright regarding life history, disease transmission, and con- blue with pronounced markings on the head, scutel- trol strategies has focused on populations from north- lum, and wings (Severin 1949). Whether these differ- ern California (Severin 1949, Purcell 1976, Feil et al. ences in morphology are an expression of phenotypic plasticity or are indicative of genetic differences is 1 Department of Entomology, University of California, Riverside, currently unknown. However, this latter possibility CA 92521. could have important implications for the direction of 2 Center for Invasive Species Research, University of California, Riverside, CA 92521. current research and the tactics presently used 3 Corresponding author, e-mail: [email protected]. throughout California for control of this vineyard pest. 0022-0493/11/0279Ð0287$04.00/0 ᭧ 2011 Entomological Society of America 280 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 1 Fig. 1. Photograph of three G. atropunctata specimens illustrating the differences in morphology among populations in California. (A) Southern California, Laguna Beach. (B) Central California, Berkeley. (C) Northern California, Redding. (Online Þgure in color.) Its large range, disjunct distribution, and occupation collected in Fullerton, CA, and three specimens of G. of isolated habitats, suggest that populations of G. flavovittata were collected in Uruapan, Michoaca´n, atropunctata across California may have quantiÞable Mexico (Table 1; Fig. 2). All specimens collected for population-level genetic differences. Given its status study were preserved in 95% ethanol, and kept at as a signiÞcant pest, such genetic differentiation may Ϫ20ЊC until used for DNA analyses. Voucher speci- have important ramiÞcations for the control of any mens of each Graphocephala species were deposited in given population. We examined differences among the University of CaliforniaÐRiverside Entomology G. atropunctata Californian populations of along a lat- Museum (Table 1). itudinal cline of Ϸ1,000 km, by using DNA sequence data from nuclear and mitochondrial genes to assess gene ßow between study populations. This work had three main objectives. The Þrst was to examine DNA sequences from different G. atropunctata populations for evidence of the existence of cryptic species. Sec- ond, we sought to examine molecular level differences in G. atropunctata populations across California to ascertain the likely level of interpopulation movement and gene ßow. Third, we compared G. atropunctata to two other species of Graphocephala, Graphocephala cythura Baker and Graphocephala flavovittata Metcalf (Fig. 2), to determine molecular similarity between these three species. The results of these studies are presented here. Materials and Methods Specimen Collections. G. atropunctata were col- lected between July 2007 and January 2008 from lo- cations throughout California across a latitudinal range of Ϸ1,000 km. Adult specimens of G. atropunc- tata were collected from 23 locations across coastal and inland southern California, the central coast, the central valley, the San Francisco Bay area, Napa and Sonoma valleys, and coastal and inland northern Cal- ifornia (Table 1; Fig. 3). Sample locations were sep- Fig. 2. Photographs of G. cythura (A) and G. flavovittata arated by at least 3 km. Two additional species of (B) illustrating morphology, in particular, color and body Graphocephala were collected for DNA comparison to markings, for comparison with G. atropunctata (see Fig. 1). G. atropunctata. Two specimens of G. cythura were (Online Þgure in color.) February 2011 BALLMAN ET AL.: POPULATION GENETICS OF G. atropunctata IN CALIFORNIA 281 Table 1. Collection and voucher information for populations of Graphocephala spp. studied Collection date Elevation California Map GPS coordinates a Species b UCRC ENT accession no. (mo/d/yr) (m) county reference 7/15/2007 33Њ 32Ј33Љ N 117Њ 47Ј07Љ W 0 Orange G. atropunctata S 223957, 223956, 223955, 015808*, 015809* 7/17/2007 33Њ 29Ј29Љ N 117Њ 15Ј09Љ W 306 Riverside G. atropunctata T 223954, 223953, 015819* 7/30/2007 37Њ 52Ј39Љ N, 122Њ 14Ј40Љ W 309 Alameda G. atropunctata J 223946, 223945, 223944, 015810*, 015811* 7/30/2007 37Њ 53Ј08Љ N, 122Њ 15Ј42Љ 146 Alameda G. atropunctata I 223943, 223942, 223941 7/30/2007 38Њ 30Ј29Љ N, 122 53Ј09Љ W 30 Sonoma G. atropunctata H 223940, 223939, 223938, 015812*, 015813* 7/30/2007 38Њ 35Ј39N, 122Њ 55Ј0Љ W 155 Sonoma G. atropunctata G 223937, 223936, 223935 7:1:2007 40Њ 40Ј60Љ N, 122Њ 39Ј00Љ W 767 Shasta G. atropunctata C 223930, 223929, 223928 7/31/2007 38Њ 53Ј48Љ N,
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