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DNA Barcodes Affirm That 16 Species of Apparently Generalist Tropical DNA barcodes affirm that 16 species of apparently SEE COMMENTARY generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists M. Alex Smith*†, D. Monty Wood‡, Daniel H. Janzen†§, Winnie Hallwachs§, and Paul D. N. Hebert* *Biodiversity Institute of Ontario, University of Guelph, Guelph, ON, Canada N1G 2W1; ‡Diptera Unit, Canadian National Collection of Insects, Agriculture and Agri-Food Canada, Ottawa, ON, Canada K1A 0C6; and §Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018 Contributed by Daniel H. Janzen, December 30, 2006 (sent for review December 26, 2006) Many species of tachinid flies are viewed as generalist parasitoids exceptions are truly generalists, we cytochrome c oxidase 1 (CO1) because what is apparently a single species of fly has been reared DNA-barcoded (e.g., as in ref. 12) the 16 most generalist mor- from many species of caterpillars. However, an ongoing inventory of phospecies, all being species that have been reared by the inventory the tachinid flies parasitizing thousands of species of caterpillars in from many species of caterpillars in a few to many families and all Area de Conservacio´ n Guanacaste, northwestern Costa Rica, has being species reared tens to hundreds of times [see supporting encountered >400 species of specialist tachinids with only a few information (SI) Table 1 and SI Appendices 1 and 2] . When generalists. We DNA-barcoded 2,134 flies belonging to what ap- barcoded, this select group of exceptionally generalist morphospe- peared to be the 16 most generalist of the reared tachinid morphospe- cies dissolved into 64 species of specialists and 9 generalists (Fig. 1 cies and encountered 73 mitochondrial lineages separated by an and SI Table 1). This outcome mirrors and magnifies the result average of 4% sequence divergence. These lineages are supported by recorded when we barcoded the 20 relatively specialist morphospe- collateral ecological information and, where tested, by independent cies of Belvosia, another tachinid genus living in the same ACG nuclear markers (28S and ITS1), and we therefore view these lineages habitats; its three somewhat generalist species were each found to as provisional species. Each of the 16 apparently generalist species be complexes of specialists (12). dissolved into one of four patterns: (i) a single generalist species, (ii) As of October 2006, the ACG caterpillar and parasitoid inventory a pair of morphologically cryptic generalist species, (iii) a complex of had reared tachinid flies from 16,500 of Ͼ390,000 wild-caught specialist species plus a generalist, or (iv) a complex of specialists with caterpillars (Ϸ4.2% rate of infection). For the past 17 years, no remaining generalist. In sum, there remained 9 generalist species D.M.W. (8, 13) has iteratively assigned these flies to morphospecies among the 73 mitochondrial lineages we analyzed, demonstrating and identified them with scientific names when available. The first that a generalist lifestyle is possible for a tropical caterpillar parasitoid taxonomic assignment was completed without knowledge of the fly. These results reinforce the emerging suspicion that estimates of host caterpillar. Taxonomic assignments were flagged for reexam- global species richness are likely underestimates for parasitoids ination when the fly’s host caterpillar species did not match what (which may constitute as much as 20% of all animal life) and that the appeared to be the host-use pattern of that fly species. Although all strategy of being a tropical generalist parasitic fly may be yet more flies were placed to genus (described or undescribed), Ͻ10% of the unusual than has been envisioned for tachinids. morphospecies appeared to match a known type specimen and thus could be presently “named” with any confidence. Inasmuch as it is 28S ͉ Area de Conservacio´ n Guanacaste ͉ cytochrome c oxidase 1 ͉ believed that only 7–20% of insect species have been scientifically internal transcribed spacer 1 ͉ species diversity described (3, 14), such a low level of taxonomic allocation is not surprising. However, all of the 16 most generalist morphospecies arasitoid insects are currently believed to comprise as much as were sufficiently distinctive among the hundreds of species-, genus-, Pone quarter of all insect species (1, 2) and, because insects or family-level specialists that they did receive a tentative scientific comprise Ϸ80% of all named animal species, up to 20% of all name through this process; on average, these names are all Ͼ100 animal life (3). However, accurate evaluations of parasitoid species years old (SI Table 2). We then added sequence data from CO1 richness (2), and subsequent determinations of parasitoid host- barcoding to the 16 morphologically defined and host-checked units specificity, are impeded by the very large number of morphologi- already recognized to determine whether each generalist mor- cally similar species and the resultant difficulty in identifying them. phospecies comprised specimens with little intraspecific barcode This situation further complicates the determination of host– variability. Such a protocol determines whether these 16 species can parasitoid relationships. There may be many more species of insect ECOLOGY parasitoids than currently believed if host-specificity has been underestimated (4, 5). After the Hymenoptera, Diptera (flies) are Author contributions: M.A.S., D.H.J., W.H., and P.D.N.H. designed research; M.A.S., D.M.W., the most species-rich group of parasitoids, and the obligate para- D.H.J., and W.H. performed research; M.A.S., D.H.J., and W.H. analyzed data; and M.A.S., D.H.J., W.H., and P.D.N.H. wrote the paper. sitoid family Tachinidae is among the most species-rich of Diptera families, with nearly 10,000 described species (1, 6–8). Within this The authors declare no conflict of interest. diversity, many described species of Tachinidae are extremely Freely available online through the PNAS open access option. similar morphologically, and it is a taxonomically challenging Abbreviations: ACG, Area de Conservacio´ n Guanacaste, Costa Rica; CO1, cytochrome c family. oxidase 1; NJ, neighbor-joining. It is a widely held view that many species of tachinid parasitoids Data deposition: The sequences reported in this paper have been deposited in the GenBank database (CO1: accession nos. EF180450–EF182583; 28S and ITS1: accession nos. EF183546– are relatively generalist (polyphagous) in the species of hosts they EF184019 and EF189688–EF189703 and two representative sequences of Chetogena scute- parasitize (7–10). However, a 29-year inventory of Ͼ400 species of llarisDHJ01 Wolbachia, accession nos. EF192042 and EF192043). tachinids reared from Ͼ390,000 wild-caught caterpillars of Ͼ3,500 See Commentary on page 4775. species in Area de Conservacio´n Guanacaste (ACG) in northwest- †To whom correspondence may be addressed. E-mail: [email protected] or djanzen@ ern Costa Rica indicates that at least 90% of the tachinid species sas.upenn.edu. from this tropical site are host-specific to one or a few related This article contains supporting information online at www.pnas.org/cgi/content/full/ species (specialists) (ref. 11 and http://janzen.sas.upenn.edu). How- 0700050104/DC1. ever, there are conspicuous exceptions. To ascertain whether these © 2007 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0700050104 PNAS ͉ March 20, 2007 ͉ vol. 104 ͉ no. 12 ͉ 4967–4972 1 % Winthemia tricolorDHJ01 Arctiidae (1) Winthemia tricolorDHJ02 Arctiidae (1) Winthemia tricolorDHJ04 Geometridae (1) Winthemia tricolorDHJ03 Geometridae (1) Hemisturmia tenuipalpisDHJ01 Immidae (1) Hemisturmia tenuipalpisDHJ02 Saturnidae (1) Hemisturmia tenuipalpisDHJ03 5 families (10) Hemisturmia tenuipalpisDHJ04 Crambidae (1) Anoxynops auratusDHJ03 Nymphalidae (1) Anoxynops auratusDHJ06 Nymphalidae (1) Anoxynops auratusDHJ08 Nymphalidae (1) Anoxynops auratusDHJ07 Nymphalidae (1) Anoxynops auratusDHJ05 Nymphalidae (1) Anoxynops auratusDHJ04 Nymphalidae (1) Anoxynops auratusDHJ11 Sphingidae (1) Anoxynops auratusDHJ01 Nymphalidae (1) Hyphantrophaga blandaDHJ06 7 families (21) Hyphantrophaga blandaDHJ03 Crambidae (3) Hyphantrophaga blandaDHJ02 Geometridae (1) Hyphantrophaga virilis 22 families (176) Patelloa xanthuraDHJ01 19 families (145) Patelloa xanthuraDHJ03 -Papilionidae (3) Patelloa xanthuraDHJ02 Papilionidae (1) Patelloa xanthuraDHJ04 Hesperidae (6) Patelloa xanthuraDHJ06 Limacodidae (1) Patelloa xanthuraDHJ05 3 families (6) Lespesia parviteresDHJ06 Hesperidae (6) Lespesia parviteresDHJ01 Pieridae (2) Lespesia parviteresDHJ04 Riodinidae (4) Lespesia parviteresDHJ02 Noctuidae (1) Lespesia posticaDHJ07 3 families (5) Lespesia posticaDHJ05 Noctuidae (2) Lespesia posticaDHJ06 Noctuidae (6) Lespesia posticaDHJ08 - 1 sp Noctuidae Lespesia posticaDHJ01 Notodontidae (2) Lespesia posticaDHJ11 Noctuidae (1) Lespesia aletiae - 12 families (66) Siphosturmia rafaeliDHJ04 - Hesperidae (1) Siphosturmia rafaeliDHJ03 - Hesperidae (10) Siphosturmia rafaeliDHJ01 - Hesperidae (1) Siphosturmia rafaeliDHJ05 - Hesperidae (2) Siphosturmia rafaeliDHJ02 - Hesperidae (8) Siphosturmia rafaeliDHJ06 - Hesperidae (3) Drino piceiventrisDHJ03 - Sphingidae (1) Drino piceiventrisDHJ05 - Sphingidae (12) Drino piceiventrisDHJ07 - Sphingidae (5) Drino piceiventrisDHJ06 - Sphingidae (5) Drino piceiventrisDHJ04 - Sphingidae (1) Drino piceiventrisDHJ13 - Sphingidae (2) Drino piceiventrisDHJ18 - Sphingidae (2) Drino piceiventrisDHJ17 - Sphingidae (2) Drino piceiventrisDHJ10 - Sphingidae (5)
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