Vector-Host Interactions of Culex Pipiens Complex in Northeastern and Southwestern USA Author(S): Goudarz Molaei , Shaoming Huang and Theodore G

Vector-Host Interactions of Culex pipiens Complex in Northeastern and Southwestern USA Author(s): Goudarz Molaei , Shaoming Huang and Theodore G. Andreadis Source: Journal of the American Mosquito Control Association, 28(4s):127-136. 2012. Published By: The American Mosquito Control Association DOI: http://dx.doi.org/10.2987/8756-971X-28.4s.127 URL: http://www.bioone.org/doi/full/10.2987/8756-971X-28.4s.127 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. Copyright E 2012 by The American Mosquito Control Association, Inc. VECTOR-HOST INTERACTIONS OF CULEX PIPIENS COMPLEX IN NORTHEASTERN AND SOUTHWESTERN USA 2 GOUDARZ MOLAEI,1 SHAOMING HUANG AND THEODORE G. ANDREADIS1 ABSTRACT. Studies on the vector-host interactions of Culex pipiens complex mosquitoes by sequencing portions of mitochondrial cytochrome b gene indicate that Cx. p. pipiens f. pipiens predominantly feed on avian hosts (93.1%), and focus feeding activity on several key bird species, in particular the American robin, the gray catbird, and the house sparrow in Connecticut. However, Cx. p. quinquefasciatus indiscriminately feed on both birds and mammals. Culex p. quinquefasciatus in Harris County - Texas and southern California acquired 39.1% and 88.2% of bloodmeals from birds, respectively. Mammalian-derived bloodmeals constituted 52.5% and 9.6% in the two regions, respectively. The most frequent avian hosts for this mosquito species in the southwestern U.S. were the mourning dove, the white-winged dove, the house sparrow and the house finch. Humans infrequently served as the source of bloodmeals for Cx. p. pipiens and Cx. p. quinquefasciatus. Microsatellite analysis of mosquitoes from Chicago, Illinois showed that Cx. p. pipiens f. pipiens with mammalian- derived bloodmeals had significantly higher ancestry and proportion of hybrids from Cx. p. pipiens f. molestus than did those with avian-derived bloodmeals. KEY WORDS Culex pipiens complex, blood-feeding patterns, mitochondrial cytochrome b gene, microsatellite analysis, hybrid ancestry INTRODUCTION California) U.S. (Molaei et al. 2006, 2007, 2010) (Fig. 1). We also reviewed studies on the genetic The Culex pipiens complex in North America structure and potential influence of introgressions consists of Cx. p. pipiens (L.) form pipiens, Cx. p. on the blood feeding behavior of Cx. p. pipiens in pipiens f. molestus, Cx. p. quinquefasciatus Say, northeastern and midwestern U.S. (Huang et al. and hybrids between Cx. p. pipiens f. pipiens and 2008, 2009). Cx. p. quinquefasciatus (Barr 1957). As principal vectors of several disease-causing pathogens, including West Nile virus (WNV) and St. Louis Culex. p. pipiens form pipiens virus (Mitchell et al. 1980, Hayes et al. 2005, Savage et al. 2007), members of the complex Studies on the vector-host interactions and exhibit substantial diversity in physiology, behav- blood feeding patterns of Cx. p. pipiens f. pipiens ior and geographic distribution. populations from north temperate regions of the U.S. have shown that these mosquitoes readily Knowledge of the vector-host interactions and feed on avian hosts and focus blood feeding host feeding patterns of Culex pipiens complex in activity on several key bird species, in particular nature is essential for evaluating their vectorial Passeriformes, that are capable of harboring capacity and for assessing the role of various vertebrates as reservoir and amplifying hosts arboviruses (Apperson et al. 2002, 2004; Kilpa- for vector-borne zoonotic pathogens. Although trick et al. 2006; Molaei et al. 2006; Savage et al. earlier studies using serologic techniques have 2007; Hamer et al. 2008). An analyses of engorged provided valuable information on the blood fee- Cx. p. pipiens f. pipiens from Connecticut, for ding patterns of Cx. pipiens complex, recent example, revealed that 93.1% of these mosquitoes advances in molecular techniques using polymer- acquired bloodmeals from avian hosts only, 2.5% ase chain reaction-based assays have permitted from mammalian, 0.5% from amphibian, and the identification of hosts to the species level with 3.9% from both avian and mammalian hosts a much higher degree of accuracy. (Fig. 2) (Molaei et al. 2006). In a recent study of As part of ongoing efforts to better understand Cx.p.pipiensfrom Sacramento and Yolo the vector potentials of mosquito species in trans- Counties in California, an overwhelming majority mission of arboviruses, we reviewed studies on (. 99%) were identified as having avian-derived the host feeding patterns of Cx. pipiens complex bloodmeals, though the genetic identities of these in the northeastern (Connecticut) and south- mosquitoes and degrees of introgressions with western (Harris County - Texas and southern other members of the Cx. pipiens complex were not determined (Montgomery et al. 2011). How- 1 ever, considerable geographic variation in the Center for Vector Biology and Zoonotic Diseases, host-selection patterns of Cx. p. pipiens f. pipiens The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, CT 06511. populations has been reported throughout their 2 San Joaquin County Mosquito and Vector Control range of distribution in the U.S. Studies in more District, 7759 South Airport Way Stockton, CA 95206- southern and midwestern regions have shown 3918. that a substantial number of individuals fed on 127 128 CULEX PIPIENS COMPLEX SYMPOSIUM VOL.28,SUPPLEMENT TO NO.4 Fig. 1. Collection sites of blood-fed (A) Cx. p. pipiens (n 5 15 sites) in Chicago, Illinois, 2005–2006, (B) Cx. p. pipiens (n 5 31 sites) in Connecticut, 2002–2004, (C) Cx. p. quinquefasciatus (n 5 69 sites) in Orange, Riverside, and San Bernardino Counties, southern California, 2006–2008, (D) Cx. p. quinquefasciatus (n 5 268 sites) in Harris County, Texas, 2005. (Panel A courtesy of Dr. Gabriel L. Hamer.) mammals including humans: Washington DC and mourning dove, Zenaida macroura (L.) (6.1%), Maryland - 13% (Kilpatrick et al. 2006), Chicago, and a few other mostly Passeriformes birds were Illinois - 22.4% (Hamer et al. 2008), Tennessee identified as the most frequent hosts for Cx. p. -24% (Apperson et al. 2004), and New Jersey pipiens f. pipiens in Connecticut (Molaei et al. -38% (Apperson et al. 2004). 2006) (Fig. 3). Avian hosts of Cx. p. pipiens f. pipiens: Several Populations of American robins use a wide studies have reported American robins as the most variety of open and forested habitats in urban/ frequent hosts for Cx. p. pipiens f. pipiens from suburban and rural settings throughout most of various regions in the U.S. (Apperson et al. 2002, North America (Martin 1973, Hutto 1995). These 2004; Kilpatrick et al. 2006; Molaei et al. 2006; birds are competent amplifying hosts for arbovi- Hamer et al. 2008; Montgomery et al. 2011). ruses including WNV and eastern equine enceph- Among 27 avian species, the American robin, alitis virus (EEEV), based on the intensity of Turdus migratorius Linnaeus (37.7% of all verte- infection and duration of viremias (Komar et al. brate-derived bloodmeals), the gray catbird, 1999, 2003). Furthermore, WNV and EEEV have Dumetella carolinensis (L.) (10.4%), the house been isolated from wild American robins and sparrow, Passer domesticus (L.) (9.9%), the Euro- antibody prevalence studies indicate that these pean starling, Sturnus vulgaris L. (6.6%), the birds are frequently exposed to the aforementioned HOST SELECTION OF CULEX PIPIENS COMPLEX 129 Fig. 2. Proportion of vertebrate blood meals for Cx. p. pipiens from Connecticut, and Cx. p. quinquefasciatus from Harris County in Texas, and from Orange, Riverside, and San Bernardino Counties in southern California. viruses (Dalrymple et al. 1972, Bast et al. 1973, arboviruses throughout their range of distribution Morris et al. 1975, Main et al. 1988, Crans et al. in the U.S. 1994, Komar et al. 2001, Hamer et al. 2009, Kent et Mammalian hosts of Cx. p. pipiens f. pipiens: al. 2009). These findings highlight the importance Although infrequent, 7 mammalian species were of American robins in the amplification of identified as the source of bloodmeals for this Fig. 3. Percentage of avian- and mammalian-derived blood meals identified from Cx. p. pipiens (n5 204) in Connecticut, 2002–2004. 130 CULEX PIPIENS COMPLEX SYMPOSIUM VOL.28,SUPPLEMENT TO NO.4 mosquito species in Connecticut (Molaei et al. Analysis of 415 engorged Cx. p. quinquefasciatus 2006). Human-derived bloodmeals were infre- from southern California (Molaei et al. 2010) has quently detected (0.5%), whereas white-tailed shown that 88.2%, 9.6%, and 2.2% of mosquitoes deer, Odocoileus virginianus Zimmermann was acquired bloodmeals from birds, mammals, and the most

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