Genomics-based taxonomic rearrangement of Achlyodini and Carcharodini (Lepidoptera: Hesperiidae: Pyrginae)
Jing Zhang
Eugene McDermott Center for Human Growth and Development and Department of Biophysics University of Texas Southwestern Medical Center 5323 Harry Hines Blvd., Dallas, TX, 75390-8816 USA
Qian Cong
Eugene McDermott Center for Human Growth and Development and Department of Biophysics University of Texas Southwestern Medical Center 5323 Harry Hines Blvd., Dallas, TX, 75390-8816 USA
Jinhui Shen
Department of Biophysics University of Texas Southwestern Medical Center 5323 Harry Hines Blvd., Dallas, TX, 75390-9050 USA
Leina Song
Department of Biophysics University of Texas Southwestern Medical Center 5323 Harry Hines Blvd., Dallas, TX, 75390-9050 USA
Nick V. Grishin
Departments of Biophysics and Biochemistry University of Texas Southwestern Medical Center 5323 Harry Hines Blvd., Dallas, TX, 75390-9050 USA
Abstract
Genomic analysis of Pyrginae Burmeister, 1878 (Lepidoptera: Hesperiidae Latreille, 1809) with an emphasis on the tribes Achlyodini Burmeister, 1878 and Carcharodini Verity, 1940 reveals many incon¬sistencies between the resulting phylogeny and the current classification. These problems are corrected by proposing new taxa, changing the ranks of others, or synonymizing them, and transferring species between genera. As a result, five subtribes, one genus, 20 subgenera, and one species are proposed as new: Cyclo¬semiina Grishin, new subtribe (type genus Cyclosemia Mabille, 1878), Ilianina Grishin, new subtribe (type genus Iliana E. Bell, 1937), Nisoniadina Grishin, new subtribe (type genus Nisoniades Hübner, [1819]), Burcina Grishin, new subtribe (type genus Burca E. Bell and W. Comstock, 1948), and Pholisorina Grishin, new subtribe (type genus Pholisora Scudder, 1872), all in Carcharodini; Lirra Grishin, new genus (type species Leucochitonea limaea Hewitson, 1868) in Pythonidina Grishin, 2019; Trifa Grishin, new subgenus (type species Tagiades jacobus Plötz, 1884), Tuberna Grishin, new subgenus (type species Pythonides contu¬bernalis Mabille, 1883), Ebona Grishin, new subgenus (type species Quadrus eboneus E. Bell, 1947), Noctis Grishin, new subgenus (type species Achlyodes accedens Mabille, 1895), and Cyrna Grishin, new subgenus (type species Achlyodes cyrna Mabille, 1895) of Quadrus Lindsey, 1925; Liddia Grishin, new subgenus (type species Helias pallida R. Felder, 1869), Minna Grishin, new subgenus (type species Achlyodes minna Evans, 1953), and Thilla Grishin, new subgenus (type species Eurypterus later Mabille, 1891) of Eantis Boisdu¬val, 1836; Torgus Grishin, new subgenus (type species Ouleus gorgus E. Bell, 1937) of Iliana E. Bell, 1937; Fenops Grishin, new subgenus (type species Cabares enops Godman and Salvin, 1894) of Polyctor Evans, 1953; Bezus Grishin, new subgenus (type species Pellicia bessus Möschler, 1877) and Macarius Grishin, new subgenus (type species Pellicia macarius Herrich-Schäffer, 1870) of Nisoniades Hübner, [1819]; Quadralis Grishin, new subgenus (type species Pterygospidea extensa Mabille, 1891) of Gorgopas Godman and Salvin, 1894; Menuda Grishin, new subgenus (type species Nisoniades menuda Weeks, 1902) and Narycus Grishin, new subgenus (type species Pythonides narycus Mabille, 1889) of Perus Grishin, 2019; Bovaria Grishin, new subgenus (type species Achlyodes cyclops Mabille, 1876), Sebia Grishin, new subgenus (type species Niso¬niades eusebius Plötz, 1884), and Stolla Grishin, new subgenus (type species Pholisora balsa E. Bell, 1937) of Bolla Mabille, 1903; Vulga Grishin, new subgenus (type species Achlyodes vulgata Möschler, 1879) and Capilla Grishin, new subgenus (type species Helias aurocapilla Staudinger, 1876, currently a junior subjec¬tive synonym of Hesperia musculus Burmeister, 1875) of Staphylus Godman and Salvin, 1896; and Quadrus (Zera) vivax Grishin, new species (type locality in Brazil: Rio de Janeiro). The following 10 are subgenera, not genera or synonyms: Ouleus Lindsey, 1925 and Zera Evans, 1953 of Quadrus Lindsey, 1925; Atarnes Godman and Salvin, 1897 and Eburuncus Grishin, 2012 of Milanion Godman and Salvin, 1895; Pachyneuria Mabille, 1888 and Austinus O. Mielke and Casagrande, 2016 of Sophista Plötz, 1879; Hemipteris Mabille, 1889 and Mictris Evans, 1955 of Pellicia Herrich-Schäffer, 1870; and Hesperopsis Dyar, 1905 and Scantilla Godman and Salvin, 1896 of Staphylus Godman and Salvin, 1896. The following 7 are species, not subspecies: Qua-drus (Ebona) cristatus (Steinhauser, 1989) (not Quadrus (Ebona) negrus (Nicolay, 1980)), Quadrus (Quadrus) ophia (A. Butler, 1870) (not Quadrus (Quadrus) lugubris (R. Felder, 1869)), Quadrus (Zera) gellius (Mabille, 1903) and Quadrus (Zera) servius (Plötz, 1884) (not Quadrus (Zera) hyacinthinus (Mabille, 1877)), Mimia pazana Evans,1953 (not Mimia phidyle (Godman and Salvin, 1894)), Polyctor (Polyctor) dagua Evans, 1953 (not Polyctor (Polyctor) polyctor (Prittwitz, 1868)), and Staphylus (Vulga) satrap Evans, 1953 (not Staphylus (Vulga) saxos Evans, 1953); and these 8 are species, not synonyms: Quadrus (Zera) menedemus (Godman and Salvin, 1894) (not Quadrus (Zera) tetrastigma (Sepp, [1847])), Pellicia (Pellicia) bilinea Mabille, 1889 (not Pellicia (Pellicia) dimidiata Herrich-Schäffer, 1870), Pellicia (Hemipteris) nema Williams and Bell, 1939 (not Pellicia (Pellicia) theon Plötz, 1882), Bolla (Bovaria) sodalis Schaus, 1913 (not Bolla (Bolla) imbras (God¬man and Salvin, 1896)), Bolla (Bovaria) aplica (E. Bell, 1937) (not Bolla (Sebia) eusebius (Plötz, 1884)), Bolla (Sebia) chilpancingo (E. Bell, 1937) (not Bolla (Bolla) subapicatus (Schaus, 1902)), and Bolla (Stolla) madrea (R. Williams and E. Bell, 1940) and Bolla (Stolla) hazelae (Hayward, 1940) (not Bolla (Stolla) zorilla (Plötz, 1886)). The following 2 are junior subjective synonyms: Achlyodes erisichthon Plötz, 1884 of Quadrus (Zera) servius (Plötz, 1884) (not a subspecies of Quadrus (Zera) tetrastigma (Sepp, [1847]) and Staphylus subapica¬tus Schaus, 1902 of Bolla (Bolla) imbras (Godman and Salvin, 1896). Furthermore, we propose the following additional new genus-species combination: Gindanes homer (Evans, 1953), Gindanes nides (O. Mielke and Casagrande, 2002), Gindanes maraca (O. Mielke and Casagrande, 1992), Gindanes jenmorrisae (Shuey and Ramírez. 2022), Gindanes tullia (Evans, 1953), Gindanes herennius (Geyer, [1838]), Gindanes proxenus (God¬man and Salvin, 1895), Gindanes parallelus (Mabille, 1898), Gindanes braga (Evans, 1953), Gindanes hampa (Evans, 1953), Gindanes rosa (Steinhauser, 1989), Gindanes neivai (Hayward, 1940), Gindanes mundo (H. Freeman, 1979), Gindanes eminus (E. Bell, 1934), Quadrus (Trifa) francesius Freeman, 1969, Quadrus (Trifa) ineptus (Draudt, 1922), Quadrus (Trifa) jacobus (Plötz, 1884), Quadrus (Tuberna) lancea (Hewitson, 1868), Quadrus (Ebona) pescada (E. Bell, 1956), Lirra pteras (Godman and Salvin, 1895), and Lirra limaea (Hewit¬son, 1868) (not Pythonides Hübner, 1819); Quadrus (Cyrna) zora (Evans, 1953) (not Bolla Mabille, 1903); Eantis later (Mabille, 1891) and Eantis haber (Mabille, 1891) (not Aethilla Hewitson, 1868); Iliana (Torgus) gorgus (E. Bell, 1937) and Iliana (Torgus) taurus (Evans, 1953) (not Eantis Boisduval, 1836); Bolla (Stolla) evemerus (Godman and Salvin, 1896), Bolla (Stolla) chlora (Evans, 1953), Bolla (Stolla) astra (R. Williams and E. Bell, 1940), Bolla (Stolla) balsa (E. Bell, 1937), Bolla (Stolla) tridentis (Steinhauser, 1989), Bolla (Stolla) esmeraldus (L. Miller, 1966), Bolla (Stolla) chlorocephala (Latreille, [1824]), and Bolla (Stolla) incanus (E. Bell, 1932) (not Staphylus Godman and Salvin, 1896). Finally, lectotypes are designated for Achlyodes servius Plötz, 1884 (type locality in Brazil: Rio de Janeiro), Pellicia theon Plötz, 1882 (type locality in South America), and Nisoniades eusebius Plötz, 1884 (type locality in Central America). Unless stated otherwise, all subgen¬era, species, subspecies, and synonyms of mentioned genera and species are transferred with their parent taxa, and others remain as previously classified.
References
- Bachtrog D, Thornton K, Clark A, Andolfatto P. 2006. Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution 60(2): 292–302.
- Buchfink B, Xie C, Huson DH. 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods 12(1): 59–60.
- Burns JM, Janzen DH, Hajibabaei M, Hallwachs W, Hebert PD. 2008. DNA barcodes and cryptic species of skipper butterflies in the genus Perichares in Area de Conservacion Guanacaste, Costa Rica. Proceedings of the National Academy of Sciences of the United States of America 105(17): 6350–6355.
- Cong Q, Shen J, Borek D, Robbins RK, Opler PA, Otwinowski Z, Grishin NV. 2017. When COI barcodes deceive: complete genomes reveal introgression in hairstreaks. Proceedings of the Royal Society B: Biological Sciences 284(1848): 20161735.
- Cong Q, Shen J, Zhang J, Li W, Kinch LN, Calhoun JV, Warren AD, Grishin NV. 2021. Genomics reveals the origins of historical specimens. Molecular Biology and Evolution 38(5): 2166–2176.
- Cong Q, Zhang J, Grishin NV. 2019a. Genomic determinants of speciation [Preprint]. bioRxiv BIORXIV/2019/837666. Available at https://www.biorxiv.org/content/10.1101/837666v1 (Last accessed November 2023.)
- Cong Q, Zhang J, Shen J, Grishin NV. 2019b. Fifty new genera of Hesperiidae (Lepidoptera). Insecta Mundi 0731: 1–56.
- Evans WH. 1953. A catalogue of the American Hesperiidae indicating the classification and nomenclature adopted in the British Museum (Natural History). Part III. Pyrginae. Section 2. The Trustees of the British Museum (Natural History); London. v + 246 p., pls. 26–53.
- Fan X, Chiba H, Huang Z, Fei W, Wang M, Safian S. 2016. Clarification of the phylogenetic framework of the tribe Baorini (Lepidoptera: Hesperiidae: Hesperiinae) inferred from multiple gene sequences. PLoS One 11(7): e0156861.
- Godman FD. 1907. Notes on the American species of Hesperiidae described by Plötz. Annals and Magazine of Natural History (7)20(16): 132–155.
- Grishin NV. 2012. Uncus shaped akin to elephant tusks defines a new genus for two very different-in-appearance Neotropical skippers (Hesperiidae: Pyrginae). The Journal of Research on the Lepidoptera 45: 101–112.
- Hebert PD, Cywinska A, Ball SL, deWaard JR. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences 270(1512): 313–321.
- Hemming AF. 1967. The generic names of the butterflies and their type-species (Lepidoptera: Rhopalocera). Bulletin of the British Museum (Natural History). Entomology Suppl. 9: 1–509.
- Huang Z-F, Chiba H, Jin J, Kizhakke AG, Wang M, Kunte K, Fan X-L. 2019. A multilocus phylogenetic framework of the tribe Aeromachini (Lepidoptera: Hesperiidae: Hesperiinae), with implications for taxonomy and biogeography. Systematic Entomology 44(1): 163–178.
- ICZN [International Commission on Zoological Nomenclature]. 1999. International code of zoological nomenclature. Fourth edition. International Trust for Zoological Nomenclature; London. xxx + 306 p
- Lemes JRA, Siewert RR, Mielke OHH, Casagrade MM, Warren AD. 2023. Taxonomic and distributional notes on Bolla tepeca (Bell, 1942), new combination (Lepidoptera: Hesperiidae: Pyrginae). Tropical Lepidoptera Research 33(2): 102.
- Li W, Cong Q, Shen J, Zhang J, Hallwachs W, Janzen DH, Grishin NV. 2019. Genomes of skipper butterflies reveal extensive convergence of wing patterns. Proceedings of the National Academy of Sciences of the United States of America 116(13): 6232–6237.
- Lukhtanov VA, Sourakov A, Zakharov E. 2016. DNA barcodes as a tool in biodiversity research: testing pre-existing taxonomic hypotheses in Delphic Apollo butterflies (Lepidoptera, Papilionidae). Systematics and Biodiversity 14: 599–613.
- Mabille P. 1903. Lepidoptera Rhopalocera. Fam. Hesperidae. Genera Insectorum 17a: 1–78.
- Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1): 268–274.
- Plötz C. 1882. Einige Hesperiinen-Gattungen und deren Arten. Berliner entomologische Zeitschrift 26(2): 253–266.
- Plötz C. 1884. Die Hesperiinen-Gruppe der Achlyoden. Jahrbücher des nassauischen Vereins für Naturkunde 37: 1–55.
- Rambaut A. 2018. FigTree, version 1.4.4. Available at http://tree.bio.ed.ac.uk/software/figtree/ (Last accessed November 2023.)
- Sahoo RK, Warren AD, Collins SC, Kodandaramaiah U. 2017. Hostplant change and paleoclimatic events explain diversification shifts in skipper butterflies (Family: Hesperiidae). BMC Evolutionary Biology 17(1): 174.
- Sahoo RK, Warren AD, Wahlberg N, Brower AV, Lukhtanov VA, Kodandaramaiah U. 2016. Ten genes and two topologies: an exploration of higher relationships in skipper butterflies (Hesperiidae). PeerJ 4: e2653.
- Schaus W. 1913. New species of Rhopalocera from Costa Rica. Proceedings of the Zoological Society of London 1913(3): 339–367.
- Shen J, Cong Q, Borek D, Otwinowski Z, Grishin NV. 2017. Complete genome of Achalarus lyciades, the first representative of the Eudaminae subfamily of skippers. Current Genomics 18(4): 366–374.
- Toussaint EFA, Braby MF, Müller CJ, Petrie EA, Kawahara AY. 2022. Molecular phylogeny, systematics and generic classification of the butterfly subfamily Trapezitinae (Lepidoptera: Papilionoidea: Hesperiidae). Zoological Journal of the Linnean Society 195: 1407–1421.
- Toussaint EFA, Breinholt JW, Earl C, Warren AD, Brower AVZ, Yago M, Dexter KM, Espeland M, Pierce NE, Lohman DJ, Kawahara AY. 2018. Anchored phylogenomics illuminates the skipper butterfly tree of life. BMC Evolutionary Biology 18(1): 101.
- Toussaint EFA, Chiba H, Yago M, Dexter KM, Warren AD, Storer C, Lohman DJ, Kawahara AY. 2021a. Afrotropics on the wing: phylogenomics and historical biogeography of awl and policeman skippers. Systematic Entomology 46(1): 172–185.
- Toussaint EFA, Ellis EA, Gott RJ, Warren AD, Dexter KM, Storer C, Lohman DJ, Kawahara AY. 2021b. Historical biogeography of Heteropterinae skippers via Beringian and post-Tethyan corridors. Zoologica Scripta 50(1): 100–111.
- Toussaint EFA, Vila R, Yago M, Chiba H, Warren AD, Aduse-Poku K, Storer C, Dexter KM, Maruyama K, Lohman DJ, Kawahara AY. 2019. Out of the Orient: Post-Tethyan transoceanic and trans-Arabian routes fostered the spread of Baorini skippers in the Afrotropics. Systematic Entomology 44(4): 926–938.
- Warren AD, Ogawa JR, Brower AVZ. 2008. Phylogenetic relationships of subfamilies and circumscription of tribes in the family Hesperiidae (Lepidoptera: Hesperioidea). Cladistics 24(5): 642–676.
- Warren AD, Ogawa JR, Brower AVZ. 2009. Revised classification of the family Hesperiidae (Lepidoptera: Hesperioidea) based on combined molecular and morphological data. Systematic Entomology 34(3): 467–523.
- Warren BCS. 1926. Monograph of the tribe Hesperiidi (European species) with revised classification of the subfamily Hesperiinae (Palaearctic species) based on the genital armature of the males. Transactions of the entomological Society of London 74: 1–170.
- Wiemers M, Balletto E, Dincă V, Fric ZF, Lamas G, Lukhtanov V, Munguira ML, van Swaay CAM, Vila R, Vliegenthart A, Wahlberg N, Verovnik R. 2018. An updated checklist of the European Butterflies (Lepidoptera, Papilionoidea). ZooKeys 811: 9-45.
- Wiemers M, Chazot N, Wheat CW, Schweiger O, Wahlberg N. 2020. A complete time-calibrated multi-gene phylogeny of the European butterflies. ZooKeys 938: 97–124.
- Zhang J, Cong Q, Burns JM, Grishin NV. 2022a. Checking the checkered taxonomy of Plötz’s checkered skippers (Hesperiidae: Pyrgini). The Taxonomic Report of the International Lepidoptera Survey 10(5): 1–31.
- Zhang J, Cong Q, Grishin NV. 2023a. Thirteen new species of butterflies (Lepidoptera: Hesperiidae) from Texas. Insecta Mundi 0969: 1–58.
- Zhang J, Cong Q, Shen J, Brockmann E, Grishin NV. 2019a. Genomes reveal drastic and recurrent phenotypic divergence in firetip skipper butterflies (Hesperiidae: Pyrrhopyginae). Proceedings of the Royal Society B: Biological Sciences 286(1903): 20190609.
- Zhang J, Cong Q, Shen J, Brockmann E, Grishin NV. 2019b. Three new subfamilies of skipper butterflies (Lepidoptera, Hesperiidae). ZooKeys 861: 91–105.
- Zhang J, Cong Q, Shen J, Grishin NV. 2022b. Taxonomic changes suggested by the genomic analysis of Hesperiidae (Lepidoptera). Insecta Mundi 0921: 1–135.
- Zhang J, Cong Q, Shen J, Opler PA, Grishin NV. 2021. Genomics-guided refinement of butterfly taxonomy. The Taxonomic Report of the International Lepidoptera Survey 9(3): 1–54.
- Zhang J, Cong Q, Shen J, Song L, Grishin NV. 2022c. Genomic DNA sequencing reveals two new North American species of Staphylus (Hesperiidae: Pyrginae: Carcharodini). The Taxonomic Report of the International Lepidoptera Survey 10(4): 1–13.
- Zhang J, Cong Q, Shen J, Song L, Grishin NV. 2023b. Butterfly classification and species discovery using genomics. The Taxonomic Report of the International Lepidoptera Survey 11(3): 1–93.
- Zhang J, Cong Q, Shen J, Song L, Grishin NV. 2023c. A taxonomic list of the Old World genera in the subfamily Hesperiinae (Hesperiidae) arranged into tribes. The Taxonomic Report of the International Lepidoptera Survey 11(2): 1–6.
- Zhang J, Cong Q, Shen J, Song L, Grishin NV. 2023d. Supplementary information to “Genomics-based taxonomic rearrangement of Achlyodini and Carcharodini (Lepidoptera: Hesperiidae: Pyrginae).” Table S1, Table S2, and DNA sequences of exons with diagnostic characters. Available at https://osf.io//8be5h/ (Last accessed November 2023.)
- Zhang J, Dolibaina DR, Cong Q, Shen J, Song L, Mielke CGC, Casagrade MM, Mielke OHH, Grishin NV. 2023d. Taxonomic notes on Neotropical Hesperiidae (Lepidoptera). Zootaxa 5271(1): 91–114.
Publication
Published