Location: Systematic Entomology Laboratory
2023 Annual Report
Objectives
Objective 1: Conduct integrative taxonomic research that incorporates adult, immature, and molecular data to develop new and improve existing classifications of agriculturally important insects, create biosystematic databases, determine host plants, and analyze phylogenetic relationships based on next-generation sequencing, comparative morphological and bioinformatics analyses, and modern illustration methods. [NP304, C1, PS1A; C2, PS2B; C3, PS3A and 3B; C4 PS4A and 4B]
Objective 2: Generate molecular and morphological diagnostic tools that will allow stakeholders and beneficiaries (e.g. Animal and Plant Health Inspection Service, Department of Homeland Security, state departments of agriculture, foreign and domestic biological control laboratories, researchers, and citizens worldwide) to accurately identify and rank agriculturally important insects. [NP304, C1, PS1A; C2, PS2B; C3, PS3A; C4 PS4A and 4B]
Objective 3: Curate and expand through fieldwork and acquisitions the U. S. National Insect Collection to support morphological and molecular research by U.S. scientists and stakeholders worldwide and enhance pest insect diagnostics. [NP304, C3, PS3A; C2, PS2B; C3, PS3A; C4 PS4A and 4B]
Objective 4: Provide expert/authoritative identifications for early detection of potentially invasive or novel insect pests intercepted by APHIS or Homeland Security personnel at U.S. ports, and generate research associated with specimens submitted by ARS researchers for biological control research with U.S. state departments of agriculture and U.S. university scientists. [NP304, C1, PS1A; C2, PS2B; C3, PS3A and 3B; C4 PS4A and 4B]
Approach
Parasitoid and phytophagous wasps (Hymenoptera) are a species-rich and biologically diverse group of insects critical to managing pests of agriculture and natural resources. Of the various types of natural enemies, parasitoid wasps are most frequently used to control pest insects. Phytophagous wasps include plant pests and species used to control weeds. We propose to acquire and analyze morphological and molecular character data (and other biosystematic and natural history data) for beneficial and pest chalcidoid, ichneumonoid, and cynipoid wasps to (1) discover and describe new taxa, as well as discover and report new natural history data; (2) generate phylogenies to estimate evolutionary relationships and dates of divergence for lineages, and predic host range for species; (3) propose new taxonomic concepts based on hypotheses of evolutionary relationships and make corresponding nomenclatural changes; (4) redescribe taxa to reflect changes in how they are defined or report new diagnostic character states; and (5) develop tools for identifying taxa. The aforementioned will be generated through phylogenomic research on Chalcidoidea, Ichneumonoidea, Ceraphronoidea, Platygastroidea and Cynipoidea, resulted in revised classifications and species delimitations. We also propose to (1) increase access to the National Insect Collection through digitizing the Hymenoptera type collection and providing that data online, as well as the Hymenoptera ethanol collection; (2) provide authoritative identifications of hymenopterans for USDA-ARS, USDA-APHIS, and other state and federal researchers and action agencies; and (3) curate selected wasp groups in the National Insect Collection (NIC) at the Smithsonian Institution National Museum of Natural History (NMNH).
Progress Report
Progress was made on all four objectives and their sub-objectives, all of which fall under National Program 304, Crop Protection & Quarantine or 104, Veterinary, Medical and Urban Entomology.
Lepidoptera systematic research fixed the true identities of grass-feeding moths and leaf-tier moths using new molecular protocols to characterize hundred-year-old type specimens in addition to morphological structures. These species that had been misclassified for over 100 years, and the leaf-tier moth larvae are commonly intercepted on greenhouse flowers from South Africa. We identified and described the unknown species of Agnippe (as Evippe) from South America that were approved for biocontrol of Prosopis over 20 years ago in Australia. We conducted a phylogenomic analysis of Old World Stem-borers (Noctuidae: Apameini: Sesamiina) and analyzed their diversification dynamics in the context of grassland evolution and fragmentation. We revised the genus-level taxonomy of a complex group of detritivorous American moths, conducted a phylogenomic and biogeographic analysis of world Cerurinae, and described two new genera to revise the taxonomy of the North American fauna. We generated and compiled the largest genomic dataset thus far for the family Notodontidae, delimiting established subfamilies, and defining new ones, including the discovery and characterization of a new family of Noctuoidea. Lepidoptera provided diagnostic tools for leaf mining trumpet moths at the generic level worldwide and for Phycitinae moths, including the navel orangeworm, from northwestern Mexico that is important to U.S. quarantine. For curation and collection expansion via fieldwork or acquisition, Lepidoptera completed the acquisition of the large, private Albu collection of ~30,000 moths primarily from western North America and Europe that enhances the moth collection of the National Museum of Natural History. In addition to the identifications incoming from U.S. ports, Lepidoptera identified new U.S. state and county records of the invasive box tree moth recently new to the U.S. (including negative records) and identified the navel orangeworm from images and sticky traps throughout the southern U.S. in collaboration with an ARS community ecology scientist.
Hymenoptera research focused on some 200 various species of parasitic wasps associated with: stink bugs that eat major food crops in the U.S. and infest homes; flies that eat strawberry and blackberry, and other fruit; herbivorous and wood-boring insects in U.S. forests that feed on trees and kill them; plant-feeding insects in grasslands adjacent to crop fields; invasive spiders in Europe; and fire ants that disturb livestock. Along with clarifying identification, new biological attributes and host records were discovered for wasps important to agriculture and natural resources. Correct identification of biological control agents, as well as an understanding of their biological role in mitigating pestiferous species populations, is essential for making rearing and quarantine decisions in the protection of U.S. agricultural interests worldwide. Lastly, a joint project with other scientists in Canada, France, Germany, Mexico, Florida, North Carolina, Pennsylvania, and Washington DC, has resulted in the first complete phylogenomic analysis of Hymenoptera relationships, published in Nature Communication.
Coleoptera research focused on generating beetle genomic DNA extractions. Furthermore, DNA grade beetle tissues were collected to improve the taxonomic scope of each sub-objective. In addition to the progress made in the molecular laboratory, ARS researchers conducted research within a grant funded by the USDA-ARS SCINet Higher Performance Computing. The grant funded a postdoctoral associate for two years to investigate the prevalence of hybridization and introgression in agroecosystems. Both the results and bioinformatic tools developed as part of this grant will improve subsequent studies that are address prevention and control of non-native agriculturally important beetle species using genomic data. The first phylogenomic hypothesis and revision at the generic-level classification of Cossoninae (Coleotpera: Curculionidae) was substantially delayed due to reduced access to the collection and molecular laboratory during the pandemic, but progress is being made in taxon selection. A synopsis of Nearctic Baridinae genera is in progress and will be submitted for publication in FY2024. A morphological character study and data matrix is underway for Nearctic baridines; initially focusing on external characters due to constraints.
Diptera research provided a review of the nine leaf-mining fruit flies known from the U.S. and Canada, including 26 new host plant records, new distribution information, and the first record of a species introduced from Europe. Additionally, analyses of the evolutionary relationships among fruit flies (>200 of the 500 genera) and among the species of the largest and most economically important fruit fly group in the tropical Americas are progressing. Phylogenomic data were collected and analyzed in order to determine phylogenetic relationships among genera of leafmining Agromyzidae, a family containing numerous important plant pests. This resulted in a well-supported phylogeny leading to the proposal of new nomenclatural changes in the number and composition of subfamilies. Phylogenomic data were also used to investigate relationships within Phytomyza, the largest genus of agromyzids, containing numerous polyphagous pest species. To further explore patterns of host-use in pest Liriomyza leafminers, single nucleotide polymorphisms were used to assess population genomic structure, as well as host-plant associated and geographic divergence within both L. trifolii and L. sativae. These results offer insights on the evolution of host-use patterns, divergence, and specialization in Liriomyza pest species, including the findings of cryptic species and host-associated subpopulations.
Accomplishments
1. Discovery and characterization of a new family of Owlet Moths. The discovery and characterization of a new family of Owlet Moths (Noctuoidea) was completed. Noctuoidea is the largest superfamily of Lepidoptera, with over 50,000 described species, yet the relationships among the 6 currently recognized noctuoid families are poorly resolved. When compiling genomic data for one of these, the Notodontidae or Prominent Moths, we discovered that one of its component subfamilies was in fact an entirely distinct lineage outside the Notodontidae and possibly the sister group to all the remaining noctuoid families. Grass-feeding moth identities in the U.S. after more than a hundred years. A grass-feeding moth described in 1794 from the U.S. Virgin Island, St. Croix, was the name applied to a widely distributed U.S. species. An ARS researcher located at the National Museum of Natural History, Smithsonian Institution, Washington, D.C., collaborated with researchers from Switzerland, England, and Germany, to adapt molecular methods to target the barcode gene in hundred-plus-year-old type specimens located in European and American museums, and together with structural characters, fixed the identity of this group of grass-feeding species. Another species described from Bermuda in 1915 is the correct name to be applied to the more widespread North American species.
2. Hyper Diverse Subfamily of Leaf Beetles. Phylogenetic research confirmed three tribes within a hyper diverse subfamily of leaf beetles. ARS researchers in collaboration with scientists in Canada, China, and India, generated and analyzed a genomic dataset of 925 nuclear loci using Anchored Hybrid Enrichment (AHE) for 100 genera of Chrysomelidae. The resulted classification placed the enigmatic, conifer root-feeding, Synetinae as separate from subfamily Eumolpinae (known to feed on the roots of a various angiosperms). The following tribes were confirmed within Galerucinae: Alticini with 700 genera and 10,000 species, Galerucini with about 500 genera and 6,000 species and Serraticollini as evolutionary sister taxon to all remaining Galerucinae with one genus and 60 species. The memberships of tribes Alticini and Galerucini was corrected by transferring incorrectly placed genera between them. The study will be useful to biological control workers, evolutionary biologists, ecologists, and anyone interested in plant feeding beetles. ARS researchers in this subproject received two grants to further the research for this objective. First ARS researchers were awarded an Artificial Intelligence (AI) Center of Excellence Innovation Grant to develop an artificial intelligence tool to identify non-native agriculturally important leaf beetles. Specifically, the grant addresses the need for such a tool by focusing on the leaf beetle genus Epitrix, which contains quarantine species that threaten many U.S. agricultural commodities such as potatoes, tomatoes, bell peppers, and eggplants. Both a postdoctoral fellow and a technician are funded for one year through this grant. Second, ARS researchers received the FY 2023 National Plant Disease Recovery System Award from the Office of National Program. This award will fund research that will begin surveillance on viruses in non-quarantine arthropods that are intercepted at ports-of-entry.
3. Systematics of true fruit flies. Research was published on the systematics of true fruit flies, including new host plant data and descriptions of 46 previously unknown species from Bolivia, Colombia, Suriname, French Guiana, and Brazil, belonging to the largest and most economically important group of fruit flies in the American tropics (Anastrepha). Previously unknown larval characters were described for nine species. Evolutionary history of host use in a genus containing sunflower maggot was performed by ARS researchers. An evolutionary analysis of the drivers of worldwide global fruit fly invasions was carried out. Further development of an online identification tool for the more than 350 species of Anastrepha was developed to facilitate identifications by other scientists. Hundreds of samples of Anestrepha and other groups were collected from Brazil, Ecuador, Peru, and Suriname, for DNA analysis. An analysis of more than 2700 DNA barcoding sequences of Anastrepha also was completed, and the investigation of additional DNA regions for diagnostics and phylogenetic analysis continued. A subsample of species were analyzed via NextGen sequencing methods towards a phylogenetic analysis to determine evolutionary relationships of the entire family of highly damaging flies. Additional names, distribution and host plant data for fruit flies were compiled to be added to the comprehensive database available via APHIS-CPHST web site; this information is critical to APHIS-PPQ and other regulatory agencies to prevent the spread of pest species into the U.S.
4. Hymenoptera phylogenomic study. The first complete Hymenoptera phylogenomic study was published in Nature Communication. In this study, we assembled the largest time-calibrated phylogeny of Hymenoptera to date and investigated the origin and possible correlation of particular morphological and behavioral innovations with diversification in the order: the wasp waist of Apocrita; the stinger of Aculeata; parasitoidism, a specialized form of carnivory; and secondary phytophagy, a reversal to plant-feeding. ARS researchers show that parasitoidism has been the dominant strategy since the Late Triassic in Hymenoptera, but was not an immediate driver of diversification. Instead, transitions to secondary phytophagy (from parasitoidism) had a major influence on diversification rate in Hymenoptera. Support for the stinger and the wasp waist as key innovations remains equivocal, but these traits may have laid the anatomical and behavioral foundations for adaptations more directly associated with diversification.
Review Publications
Martens, A., Buffington, M.L., Quicke, D.J., Raweearamwong, M., Johnson, P.J., Butcher, B.A. 2022. Ishtarella thailandica new genus and species (Hymenoptera: Braconidae: Aphidiinae) of aphid parasitoid from Thailand, with a country checklist of Aphidiinae. Insecta Mundi. 904:1-6. https://journals.flvc.org/mundi/article/view/130216.
Norrbom, A.L., Ruiz-Arce, R., Steck, G.J., Moore, M., Wiegmann, B., Rodriguez, E.J., Branham, M., Sutton, B.D., Muller, A., Gangadin, A., Cassel, B., Ledezma, L., Troya, H., Nolazco Alvarado, N., Savaris, M., Clifford, K. 2023. Integrative approach reveals the identity of Brazilian specimens previously recognized as Anastrepha dissimilis Stone, 1942 (Diptera: Tephritidae). Zootaxa. 5228(3):317-336. https://doi.org/10.11646/zootaxa.5228.3.5.
Landry, B., Bilat, J., Hayden, J.E., Solis, M.A., Lees, D., Alvarez, N., Leger, T., Gauthier, J. 2023. The identity of Argyria lacteella (Fabricius, 1794) (Lepidoptera, Pyraloidea, Crambinae), synonyms, and related species using morphology and DNA capture in type specimens. ZooKeys. 1146:1-42. https://doi.org/10.3897/zookeys.1146.96099.
Xuan, J., Scheffer, S.J., Lonsdale, O., Cassel, B., Lewis, M.L., Eiseman, C., Liu, W., Wiegmann, B. 2022. A genome-wide phylogeny and the diversification of genus Liriomyza (Diptera: Agromyzidae) inferred from anchored phylogenomics. Systematic Entomology Laboratory World Wide Web Site. 48(1):178-197. https://doi.org/10.1111/syen.12569.
DaSilva, A., Reddy, A.M., Pratt, P.D., Hansel Friedman, M.S., Grewell, B.J., Harms, N.E., Cibils-Stewart, X., Cabrera Walsh, G., Faltlhauser, A., Chamorro, M.L. 2022. Biology of immature stages and host range characteristics of Sudauleutes bosqi (Coleoptera: Curculionidae), a candidate biological control agent of exotic Ludwigia spp. in the USA. Florida Entomologist. 105(3):243-249. https://doi.org/10.1653/024.105.0310.
Palmieri, L., Chamorro, M.L., Sharma, P.P. 2022. Phylogenetic assessment of Metamasius hemipterus species complex (Coleoptera, Curculionidae, Dryophthorinae). Molecular Phylogenetics and Evolution. 175:1-6. https://doi.org/10.1016/j.ympev.2022.107589
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Ruan, Y., Konstantinov, A.S., Damaska, A. 2022. Description of a moss-eating flea beetle Cangshanaltica fuanensis sp. nov. (Coleoptera, Chrysomelidae, Galerucinae, Alticini) from China. Journal of Insect Biodiversity. 34(2):28-32. https://doi.org/10.12976/jib/2022.34.2.1.
Solis, M.A. 2022. Cacotherapia Dyar (Pyralidae: Galleriinae) at the National Museum of Natural History, Washington, D.C.: Type images and lectotype designations. Proceedings of the Entomological Society of Washington. 124(2):346-358. https://doi.org/ 10.4289/0013-8797.124.2.346.
Goldstein, P.Z. 2022. The sterigma of Fagitana littera Guenée (Lepidoptera: Noctuidae) and its correspondence to structures in the male clasping architecture. Proceedings of the Entomological Society of Washington. 124(2):251-263. https://doi.org/10.4289/0013-8797.124.2.251.
St Laurent, R., Goldstein, P.Z., Miller, J.S., Markee, A., Staude, H., Kawahara, A.Y., Miller, S., Robbins, R. 2023. Phylogenetic systematics, diversification, and biogeography of Puss Moths and Kittens (Lepidoptera; Notodontidae; Cerurinae) and description of a new genus. Zoological Journal of the Linnean Society. 7(2):1-25. https://doi.org/10.1093/isd/ixad004.
El Harym, Y., Belqat, B., Norrbom, A.L. 2022. Host plants of fruit flies (Diptera: Tephritidae) in Morocco. Zootaxa. 5196(3):355-387. https://doi.org/10.11646/zootaxa.5196.3.3.
Konstantinov, A.S., Gultekin, L., Gultekin, N. 2023. Observations of feeding damage of some Turkish leaf beetles (Chrysomelidae) with new masquerade and host plant records. Journal of Insect Biodiversity. 37(2):40-47. https://doi.org/10.12976/jib/2023.37.2.1.
Douglas, H., Konstantinov, A.S., Brunke, A.J., Moseyko, A.G., Chapados, J.T., Eyres, J., Richter, R., Savard, K., Sears, E., Dettman, J.R., Prathapan, K.D., Ruan, Y. 2023. Phylogeny of the flea beetles (Galerucinae: Alticini) and the position of Aulacothorax elucidated through anchored phylogenomics (Coleoptera: Chrysomelidae: Alticini). Systematic Entomology. 48:1-26. https://doi.org/10.1111/syen.12582.
Van Roie, M., Clark, S., Konstantinov, A.S., Furth, D., Linzmeier, A.M. 2023. A paradox indeed: description of genitalia and clarification of the subtribal classification of Pachyonychis paradoxus Clark and Pachyonychus paradoxus Melsheimer (Coleoptera, Chrysomelidae, Galerucinae, Alticini). Journal of Insect Biodiversity. 5227(1):127-136. https://doi.org/10.11646/zootaxa.5227.1.6.
Xuan, J., Scheffer, S.J., Lewis, M.L., Cassel, B.K., Liu, W., Wiegmann, B. 2023. The phylogeny and divergence times of leaf-mining flies (Diptera: Agromyzidae) from anchored phylogenomics. Molecular Biology and Evolution. 184:Article e107778. https://doi.org/10.1016/j.ympev.2023.107778.
Schachat, S.R., Goldstein, P.Z., Desalle, R., Bobo, D., Boyce, C., Payne, J., Labandeira, C. 2022. Illusion of flight: Absence, evidence, and the age of winged insects. Biological Journal of the Linnean Society, London. 138(2):143-168. https://doi.org/10.1093/biolinnean/blac137.
Rodriguez, E.J., Steck, G.J., Moore, M., Norrbom, A.L., Diaz, J., Somma, L.A., Ruiz-Arce, R., Sutton, B.D., Nolazco Alvarado, N., Branham, M. 2022. Exceptional larval morphology of nine species of the anastrepha mucronota species group (Diptera: Tephritidae). Insect Systematics and Diversity. 1127:155-215. https://doi.org/10.3897/zookeys.1127.84628.
Chamorro, M.L., Presnall, T. 2022. Randersonia Chamorro, a new genus with two new species of North American Cryptorhynchinae (Coleoptera: Curculionidae). Zootaxa. 5222(6):591-599. https://doi.org/10.11646/zootaxa.5222.6.6.
Konstantinov, A.S., Baselga, A., Anderson, R.S., Carlton, C., Gusarov, V., Ivie, M.A., Owens, B., Sokolov, I.M., Tisheckin, A. 2023. Moss-inhabiting beetles of the West Indies (Insecta: Coleoptera). Journal of Insect Biodiversity. 38(2):48-72. https://doi.org/10.12976/jib/2023.38.2.3.
Tembrock, L., Wilson, C., Zink, F., Konstantinov, A.S., Tishechkin, A., Timm, A. 2023. CO1 barcodes resolve an asymmetric biphyletic clade for Diabrotica undecimpunctata (Coleoptera: Chrysomelidae) subspecies and provide fixed nucleotide variants for differentiation from related lineages using real-time PCR. Annals of the Entomological Society of America. 3:1-13. https://doi.org/10.3389/finsc.2023.1168586.
Kula, R.R., Aguirre, H., Rodrigues-Clavijo, P.A. 2022. A new species of Opius (Bellopius) (Hymenoptera: Braconidae) reared from Hexachaeta (Diptera: Tephritidae) flies in Colombia, with a key to New World species of Opius parasitic on fruit-infesting Tephritidae. Proceedings of the Entomological Society of Washington. 124(1):75-84. https://doi.org/10.4289/0013-8797.124.1.75.
Huang, J., Leach, H., Buffington, M.L., Rothwell, N., Wilson, J. 2023. Resident parasitoids associated with Drosophilidae in Michigan tart cherry orchards and woodland edges. Journal of Hymenoptera Research. 96:485-494. https://doi.org/10.3897/jhr.96.103160.
Santos, B., Miller Meredith, Miklasevskaja, M., Mckeown, J., Redmond, N., Coddington, J., Bird, J., Miller, S., Smith, A., Brady, S.G., Buffington, M.L., Chamorro, M.L., Dikow, T., Gates, M.W., Goldstein, P.Z., Konstantinov, A.S., Kula, R.R., Silverson, N., Solis, M.A., Naik, S., Nikolova, N., Pentinsaari, M., Prosser, S., Sones, J., Zakharov, E., Dewaard, J.R. 2023. Enhancing DNA barcode reference libraries by harvesting terrestrial arthropods at the National Museum of Natural History. Biodiversity Data Journal. 11:1-17. https://doi.org/10.3897/BDJ.11.e100904.
Blaimer, B., Santos, B., Gates, M.W., Kula, R.R., Miko, I., Rasplus, J., Smith, D.R., Talamas, E., Brady, S., Buffington, M.L. 2023. Key innovations and the diversification of Hymenoptera. Nature. 14:Article e1212. https://doi.org/10.1038/s41467-023-36868-4.