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An Evaluation of the Species Status of Bactrocera Invadens

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An Evaluation of the Species Status of Bactrocera Invadens An Evaluation of the Species Status of Bactrocera invadens and the Systematics of the Bactrocera dorsalis (Diptera: Tephritidae) Complex Author(s): Michael San Jose , Luc Leblanc , Scott M. Geib , and Daniel Rubinoff Source: Annals of the Entomological Society of America, 106(6):684-694. 2013. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/AN13017 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 An Evaluation of the Species Status of Bactrocera invadens and the Systematics of the Bactrocera dorsalis (Diptera: Tephritidae) Complex 1 1 2 1,3 MICHAEL SAN JOSE, LUC LEBLANC, SCOTT M. GEIB, AND DANIEL RUBINOFF Ann. Entomol. Soc. Am. 106(6): 684Ð694 (2013); DOI: http://dx.doi.org/10.1603/AN13017 ABSTRACT The genus Bactrocera (Tephritidae) contains Ͼ500 species, including many severe pests of fruits and vegetables. Although native to tropical and subtropical areas of Africa, India, Southeast Asia, and Australasia, a number of the pest species, largely members of the Bactrocera dorsalis (Hendel) complex, have become widespread through accidental introduction associated with agri- cultural trade. The B. dorsalis complex includes several morphologically and ecologically similar pests, making species designations uncertain. One of these, Bactrocera invadens Drew, Tsuruta, and White, endemic to Sri Lanka, has spread across Africa in the last decade and become a major agricultural pest. We sequenced one mitochondrial and two nuclear genes from 73 specimens, belonging to 19 species to construct phylogenies and examine species relationships and limits within the genus Bactrocera and several species of the B. dorsalis complexÑspeciÞcally addressing the placement of B. invadens. Results indicate the B. dorsalis complex is polyphyletic. B. invadens and several other species within the B. dorsalis complex (B. dorsalis, Bactrocera papayae Drew & Hancock, and Bactrocera philippinensis Drew & Hancock) are also paraphyletic with respect to each other and probably represent a single genetically indistinguishable, phenotypically plastic, pest species that has spread throughout the world. KEY WORDS Bactrocera dorsalis, Diptera, Tephritidae, B. invadens, invasive species The genus Bactrocera (Tephritidae) is the largest in but the most invasive and economically important the tribe Dacini, with Ͼ500 described species (Drew species belong to the Bactrocera dorsalis complex 2004, Clarke et al. 2005). It is an Old World lineage, (Clarke et al. 2005). Hardy (1969) identiÞed 11 spe- with species native to Africa, tropical and subtropical cies closely related to B. dorsalis (Hendel) and Asia, Australasia, and the western PaciÞc Islands, with grouped them in the B. dorsalis complex. Drew and the highest species diversity within Southeast Asia and Hancock (1994) published the Þrst comprehensive Australasia (Drew 2004). Bactrocera includes at least revision of the complex, describing 40 new species, 68 economically important species whose larvae infest resulting in a total of 52 species in Asia. Currently, 75 a large variety of fruit and cucurbit crops (http:// described species are considered to be part of the B. www.herbarium.hawaii.edu/fruitßy/), causing direct dorsalis complex, and many more await description damage even to unripe fruit. Many pest species have (Clarke et al. 2005). Four sibling species [B. dorsalis become widespread through accidental introductions (Hendel), Bactrocera papayae Drew & Hancock, Bac- associated with agricultural trade, and the genus now trocera philippinensis Drew & Hancock, and Bactro- occurs on every continent except Antarctica (Drew cera carambolae Drew & Hancock], herein collec- 2004). Bactrocera ßies also inßuence international tively referred to as Bactrocera dorsalis sensu lato trade; regions currently infested with Bactrocera pose (s.l.), are also among the most damaging and polypha- a signiÞcant risk to areas that are not infested. As a gous pests of the complex (Clarke et al. 2005). These result, noninfested countries severely limit or prohibit are almost identical morphologically, with minor color imports from infested areas to prevent further spread pattern differences (Drew and Hancock 1994) and of pest species. few measurable characters, the length of the female Some of the most widespread and damaging species aculeus and male aedeagus (Iwahashi 1999a,b), and of Bactrocera include Bactrocera (Zeugodacus) cucur- wing shape morphometrics (Schutze et al. 2012), to bitae (Coquillett), Bactrocera (Daculus) oleae (Gme- separate them with limited reliability. Males of most of lin), and Bactrocera (Bactrocera) tryoni (Froggatt), the B. dorsalis complex species are attracted to either of two kairomone lures, methyl eugenol (ME) or cue- 1 Department of Plant and Environmental Protection Sciences, lure (CL), although B. dorsalis s.l. species are only University of Hawaii at Manoa, 3050 Maile Way, Gilmore 310, Ho- attracted to ME, and a few species do not respond to nolulu, HI 96822. male lures. This male response has been used both as 2 U.S. Department of Agriculture PaciÞc Basin Agricultural Re- search Center, 64 Nowelo St., Hilo, HI 96720. a diagnostic tool to separate morphologically similar 3 Corresponding author, e-mail: [email protected]. species when they are attracted to different lures and 0013-8746/13/0684Ð0694$04.00/0 ᭧ 2013 Entomological Society of America November 2013 SAN JOSE ET AL.: STATUS OF B. invadens AND SYSTEMATICS OF B. dorsalis 685 as a way to monitor and control ßies in agricultural of the B. dorsalis complex, using two mitochondrial settings. and four nuclear loci. They found that several de- Understanding the evolutionary relationships of scribed pest species are paraphyletic (B. dorsalis, B. pest groups is important for many aspects of quaran- papayae, and B. philippinensis) and that B. caram- tine and control. Assessing species limits among mor- bolae was genetically distinct from the other B. phologically similar species is essential because of spe- dorsalis s.l. species. cies-centric trade policies, which inform agricultural Although Drew et al. (2008) argued that B. dorsalis quarantine decisions. Species that are morphologically s.l. comprises multiple species, recent studies by Kro- similar may have different ecological tolerances or sch et al. (2013) and Boykin et al. (2013)found no host preferences, which dictate the amount of damage evidence for distinctly different lineages separating B. they cause. dorsalis s.str., B. philippinensis, and B. papayae when B. dorsalis s.l. has invaded many places around the using microsatellites, wing shape, aedeagus length, world, including the PaciÞc (B. philippinensis in Palau; and multiple nuclear genes. A broader phylogenetic B. dorsalis in Hawaii, French Polynesia, the Mariana analysis of B. dorsalis s.l. based on multiple genes and islands [eradicated], and Nauru [eradicated]; and B. including several nonpest species should provide philippinensis and B. papayae in Australia [both erad- more insight on species limits and taxonomy. All pre- icated]) and South America (B. carambolae in Suri- vious studies with the exception of Krosch et al. (2012) name, Guyana, French Guiana, and northern Brazil). and Boykin et al. (2013) were based on relatively small They are regularly intercepted by quarantine agencies sample sizes and a limited number of mitochondrial in California and Florida, and risk of widespread es- genes. The use of only mitochondrial genes for phy- tablishment is of great concern (California Depart- logenetic reconstruction of species relationships has ment of Food and Agriculture [CDFA] 2012, Florida serious shortcomings (Funk and Omland 2003, Ballard Department of Agriculture and Consumer Services and Whitlock 2004, Cognato 2006, Rubinoff 2006). In [FDACS] 2012). In 2003, a new invasive Bactrocera our study, we used one mitochondrial gene and two species was detected attacking fruits in Kenya (Lux et nuclear genes to elucidate species relationships in the al. 2003, Drew et al. 2005), and it has rapidly spread genus Bactrocera under a phylogenetics framework. throughout tropical and subtropical Africa and is now We explored the relationship between B. invadens and encroaching on northern South Africa (De Meyer et species of the B. dorsalis complex, speciÞcally mem- al. 2010, International Plant Protection Convention bers of the B. dorsalis s.l. clade. By including several [IPPC] 2012). Described in 2005 as B. invadens Drew, noneconomic species of the B. dorsalis complex along Tsuruta, & White, this species was thought to be en- with species of economic importance, we further pro- demic to Sri Lanka,
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