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Diptera, Tachinidae) Are Not All Generalists

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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 Downloaded by guest on September 27, 2021 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)
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  • Gut Content Metabarcoding Unveils the Diet of a Flower‐Associated Coastal

    Gut Content Metabarcoding Unveils the Diet of a Flower‐Associated Coastal

    ECOSPHERE NATURALIST No guts, no glory: Gut content metabarcoding unveils the diet of a flower-associated coastal sage scrub predator PAUL MASONICK , MADISON HERNANDEZ, AND CHRISTIANE WEIRAUCH Department of Entomology, University of California, Riverside, 900 University Avenue, Riverside, California 92521 USA Citation: Masonick, P., M. Hernandez, and C. Weirauch. 2019. No guts, no glory: Gut content metabarcoding unveils the diet of a flower-associated coastal sage scrub predator. Ecosphere 10(5):e02712. 10.1002/ecs2.2712 Abstract. Invertebrate generalist predators are ubiquitous and play a major role in food-web dynamics. Molecular gut content analysis (MGCA) has become a popular means to assess prey ranges and specificity of cryptic arthropods in the absence of direct observation. While this approach has been widely used to study predation on economically important taxa (i.e., pests) in agroecosystems, it is less frequently used to study the broader trophic interactions involving generalist predators in natural communities such as the diverse and threatened coastal sage scrub communities of Southern California. Here, we employ DNA metabarcoding-based MGCA and survey the taxonomically and ecologically diverse prey range of Phymata pacifica Evans, a generalist flower-associated ambush bug (Hemiptera: Reduviidae). We detected predation on a wide array of taxa including beneficial pollinators, potential pests, and other predatory arthropods. The success of this study demonstrates the utility of MGCA in natural ecosystems and can serve as a model for future diet investigations into other cryptic and underrepresented communities. Key words: biodiversity; blocking primers; DNA detectability half-life; Eriogonum fasciculatum; food webs; intraguild predation; natural enemies. Received 24 January 2019; accepted 11 February 2019.
  • Diptera: Tachinidae: Exoristinae)

    Diptera: Tachinidae: Exoristinae)

    Two tribes hidden in one genus: the case of Agaedioxenis Villeneuve (Diptera: Tachinidae: Exoristinae) Pierfilippo Cerretti, James E. O’Hara, Isaac S. Winkler, Giuseppe Lo Giudice & John O. Stireman Organisms Diversity & Evolution ISSN 1439-6092 Org Divers Evol DOI 10.1007/s13127-015-0211-0 1 23 Your article is protected by copyright and all rights are held exclusively by Gesellschaft für Biologische Systematik. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Org Divers Evol DOI 10.1007/s13127-015-0211-0 ORIGINAL ARTICLE Two tribes hidden in one genus: the case of Agaedioxenis Villeneuve (Diptera: Tachinidae: Exoristinae) Pierfilippo Cerretti1,2 & James E. O’Hara3 & Isaac S. Winkler4 & Giuseppe Lo Giudice2 & John O. Stireman III4 Received: 18 December 2014 /Accepted: 9 March 2015 # Gesellschaft für Biologische Systematik 2015 Abstract The Afrotropical tachinid “genus” Agaedioxenis two names. Eugaedioxenis gen. nov. is recognized based on Villeneuve is taken here as an example of the challenges faced two species, Eugaedioxenis haematodes (Villeneuve), type by dipterists in classifying one of the most diverse and species species and comb.
  • Biology and Biometry of Carcelia Illota Curran (Diptera: Tachinidae) a Larval Pupal Parasitoid on Helicoverpa Armigra Hubner

    Biology and Biometry of Carcelia Illota Curran (Diptera: Tachinidae) a Larval Pupal Parasitoid on Helicoverpa Armigra Hubner

    International Journal of Scientific & Engineering Research, Volume 4, Issue 5, May-2013 2084 ISSN 2229-5518 Biology and biometry of Carcelia illota Curran (Diptera: Tachinidae), a larval pupal parasitoid on Helicoverpa armigra Hubner (Lepidoptera: Noctuidae). S.V.CHAUDHARI Abstract— Biology and biometry of Carcelia illota Curran, a larval pupal parasitoid on Helicoverpa armigera Hubner was studied. Size of egg, larvae, puparia and adults was measured. The length and width of cephalic skeleton, posterior spiracles of all three instars were measured. Duration of different life stages recorded. Size of macrotype eggs 0.65 mm 1x0.22 mm w. The newly hatched microscopic first instar larva was 0.517 mm in length and 0.11 mm width. The third instar larvae emerged from host body measured 9.413 mm in length and 2.788 mm in width. Body size, cephalic skeleton and posterior spiracles increased in length and width as larva grown. Total larval and pupal duration each recorded was about 11-12 days at 25±1°C. The body size of male and female recorded was 9.7 x 3.8 mm and 9.25 x 3.25 mm, respectively. The longevity in adults 2 to 30 days with an average of 12 days was recorded. Premating period, duration of mating, preoviposition period, oviposition period, total times for adult emergence were also recorded. Index Terms— biology, Carcelia illota, Tachinidae, Diptera, larval pupal parasitoid, pod borer Keywords - biology, biometry, Carcelia illota, Helicoverpa armigera, life stages. —————————— —————————— breeding method, mating period, preoviposition period, 1 INTRODUCTION egg laying, time for hatching, larval and pupal period in C.