Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5512 No. 3: 20 Sept. 2024
Type: Article
Published: 2024-09-20
DOI: 10.11646/zootaxa.5512.3.1
Page range: 301-342
Abstract views: 78
PDF downloaded: 4

Exochorionic morphology in four genera of Coeini: Pycina, Historis, Smyrna, and Tigridia (Nymphalidae: Nymphalinae)

Museo de Zoología (Entomología); Departamento de Biología Evolutiva; Facultad de Ciencias; Universidad Nacional Autónoma de México; México; 04510; CDMX; México
Museo de Zoología (Entomología); Departamento de Biología Evolutiva; Facultad de Ciencias; Universidad Nacional Autónoma de México; México; 04510; CDMX; México
Museo de Zoología (Entomología); Departamento de Biología Evolutiva; Facultad de Ciencias; Universidad Nacional Autónoma de México; México; 04510; CDMX; México; Posgrado en Filosofía de la Ciencia; Universidad Nacional Autónoma de México; México
Lepidoptera egg chorion ridges microstructure Neotropical region

Abstract

We describe and compare the exochorion of four species currently recognized as belonging to the nymphalid tribe Coeini: Pycina zamba zelis, Historis a. acheronta, Smyrna karwinskii, and Tigridia acesta latifascia, based on specimens collected in the field and rehydrated specimens from entomological collections. We use a staining technique and scanning electron microscopy to observe and describe the main exochorionic characters as ridges, prebasal modifications, and microstructure. We include plates with photographs, drawings, and diagrams to provide a clear visualization of these structures. We also compiled exochorionic data of other Coeini species for comparison. The eggs of Coeini share the presence of colonnade ridges with those of Nymphalini but differ from the latter in in modifications in the prebase and base, which are its distinguishing characteristics and distinct from those in Nymphalini. Exochorionic characters indicate that Coeini contains three subtribes—Pycinina, Coeina, and Coloburina—which exhibit a morphological continuum in the prebasal/basal diagnostic characters within the tribe.

 

References

  1. Alexiuk, M.R., Lalonde, M.M.L. & Marcus, J.M. (2021) Phylogenetic analysis of the complete mitochondrial genome of the Blomfild’s Beauty butterfly Smyrna blomfildia (Fabricius 1781) (Insecta: Lepidoptera: Nymphalidae). Mitochondrial DNA Part B, 6 (11), 3199–3201. https://doi.org/10.1080/23802359.2021.1989337
  2. Beccaloni, G.W., Viloria, Á.L, Hall, S.K. & Robinson, G.S (2008) Catalogue of the hostplants of the Neotropical butterflies. Monografías Tercer Milenio. Vol. 8. S.E.A. Zaragoza, 536 pp.
  3. Brown, K.S. Jr. & Freitas, A.V.L. (1994) Juvenile stages of Ithomiinae: overview and systematics (Lepidoptera: Nymphalidae). Tropical Lepidoptera, 5 (1), 9–20.
  4. Brown, K.S. Jr., Freitas, A.V.L., Wahlberg, N., Von Schoultz, B., Saura, A.O. & Saura, A. (2007) Chromosomal evolution in the South American Nymphalidae. Hereditas, 144 (4), 137–148. https://doi.org/10.1111/j.2007.0018-0661.02015.x
  5. Campos-González, E., Nieves-Uribe, S. & Llorente-Bousquets, J. (2020) Descripción del exocorion de tres especies de Coeini, Southwestern Entomologist, 45 (4), 1091–1120. https://doi.org/10.3958/059.045.0427
  6. Cole, T.C.H., Wu, Z.-Y. & Calbi, M. (2023) Urticaceae phylogeny poster (UrtPP). Available from: https://www.researchgate.net/publication/358278169_Urticaceae_Phylogeny_Poster_UrtPP_2023 (accessed 22 February 2024)
  7. De Jong, R. (2017) Fossil butterflies, calibration points and the molecular clock (Lepidoptera: Papilionoidea). Zootaxa, 4270 (1), 1–63. https://doi.org/10.11646/zootaxa.4270.1.1
  8. Dell’Erba, R., Kaminski, L.A. & Moreira, G.R.P. (2005) O estágio de ovo dos Heliconiini (Lepidoptera, Nymphalidae) do Rio Grande do Sul, Brasil. Iheringia, Série Zoologia, 95 (1), 29–46. https://doi.org/10.1590/S0073-47212005000100006
  9. Dias, F.M.S., Casagrande, M.M. & Mielke, O.H.H. (2011) External morphology and ultra-structure of eggs and first instar of Prepona laertes laertes (Hübner, [1811]), with notes on hostplant use and taxonomy. Journal of Insect Science, 11 (1), 100, 1–10. https://doi.org/10.1673/031.011.10001
  10. Döring, E.K.H. (1955) Zur Morphologie der Schmetterlingseier. Akademie-Verlag, Berlin, 154 pp., 61 pls.
  11. Espeland, M., Breinholt, J., Willmott, K.R., Warren, A.D., Vila, R., Toussaint, E.F.A., Maunsell, S.C., Aduse-Poku, K., Talavera, G., Eastwood, R., Jarzyna, M.A., Guralnick, R., Lohman, D.J., Pierce, N.E. & Kawahara, A.Y. (2018) A Comprehensive and dated phylogenomic analysis of butterflies. Current Biology, 28 (5), 770–778. https://doi.org/10.1016/j.cub.2018.01.061
  12. Flores-Gallardo, A., Llorente-Bousquets, J. & Nieves-Uribe, S. (2023) Representaciones del exocorion en morfología y sistemática de Lepidoptera: un estudio histórico-crítico sobre los estilos de imágenes científicas y virtudes epistémicas. Dugesiana, 30 (2), 117–162. https://doi.org/10.32870/dugesiana.v30i2.7312
  13. Freitas, A.V. & Brown, K.S. Jr. (2004) Phylogeny of the Nymphalidae (Lepidoptera). Systematic Biology, 53 (3), 363–383. https://doi.org/10.1080/10635150490445670
  14. Friedlander, T.P. (1985) The biology and morphology of the immature stages of Asterocampa idyja argus (Bates) (Lepidoptera: Nymphalidae). Journal of the Research on the Lepidoptera, 24 (3), 209–225. https://doi.org/10.5962/p.266786
  15. García-Barros, E. & Martín, J. (1995) The eggs of the European satyrine butterflies (Nymphalidae): external morphology and its use in systematics. Zoological Journal of the Linnean Society, 115 (1), 73–115. https://doi.org/10.1006/zjls.1995.0034
  16. Harvey, D.J. (1991) Higher classification of the Nymphalidae. Appendix B. In: Nijhout, H.F. (Ed.), The development and evolution of butterfly wing patterns. Smithsonian Institution Press, Washington, D.C., pp. 255–273.
  17. Häuser, C.L. (1893) Die inheren weiblichen Genitalorgane der Tagfalter (Rhopalocera): Vergleichende Morphologie und philogenetische Interpretarion (Insecta: Lepidoptera). Zoologische Jahrbücher. Abbteilung für Systematik, Okölogie und Geographie der Tiere, 120 (4), 389–439.
  18. Herrich-Schäffer, G.A.W. (1845) Systematische Bearbeitung der Schmetterlinge von Europa, als Text, Revision und Supplement zu J. Huebners Sammlung europäischer Schmetterlinge. Vols. 1–3. Manz, Regensburg and Berlin, 626 pp., 14 pls.
  19. Heppner, J.B. (1998) Classification of Lepidoptera. Part. 1 Introduction. Holarctic Lepidoptera, 5 (Supplement 1), i–vi + 1–148.
  20. Hernández-Mejía, C., Flores-Gallardo, A. & Llorente-Bousquets J. (2015) Morfología del corion en Leptophobia (Lepidoptera: Pieridae) e importancia taxonómica. Southwestern Entomologist, 40 (2), 351–368. https://doi.org/10.3958/059.040.0210
  21. Howe, W.H. (1975) The butterflies of North America. Doubleday & Company, Garden City, New York, 633 pp.
  22. Janz, N., Nyblom, K., Nylin, S. (2001) Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini. Evolution, 55 (4), 783–796. https://doi.org/10.1111/j.0014-3820.2001.tb00814.x
  23. Kawahara, A.Y., Storer, C., Carvalho, A.P.S., Plotkin, D.M., Condamine, F.L., Braga, M.P., Ellis, E.A., St Laurent, R.A., Li, X., Barve, V., Cai, L., Earl, C., Frandsen, P.B., Owens, H.L., Valencia-Montoya, W.A., Aduse-Poku, K., Toussaint, E.F.A., Dexter, K.M., Doleck, T., Markee, A., Messcher, R., Nguyen, Y.L., Badon, J.A.T., Benítez, H.A., Braby, M.F., Buenavente, P.A.C., Chan, W.P., Collins, S.C., Rabideau Childers, R.A., Dankowicz, E., Eastwood, R., Fric, Z.F., Gott, R.J., Hall, J.P.W., Hallwachs, W., Hardy, N.B., Sipe, R.L.H., Heath, A., Hinolan, J.D., Homziak, N.T., Hsu, Y.F., Inayoshi, Y., Itliong, M.G.A., Janzen, D.H., Kitching, I.J., Kunte, K., Lamas, G., Landis, M.J., Larsen, E.A., Larsen, T.B., Leong, J.V., Lukhtanov, V., Maier, C.A., Martinez, J.I., Martins, D.J., Maruyama, K., Maunsell, S.C., Mega, N.O., Monastyrskii, A., Morais, A.B.B., Müller, C.J., Naive, M.A.K., Nielsen, G., Padrón, P.S., Peggie, D., Romanowski, H.P., Sáfián, S., Saito, M., Schröder, S., Shirey, V., Soltis, D., Soltis, P., Sourakov, A., Talavera, G., Vila, R., Vlasanek, P., Wang, H., Warren, A.D., Willmott, K.R., Yago, M., Jetz, W., Jarzyna, M.A., Breinholt, J.W., Espeland, M., Ries, L., Guralnick, R.P., Pierce, N.E. & Lohman, D.J. (2023) A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins. Nature Ecology and Evolution, 7 (6), 903–913. https://doi.org/10.1038/s41559-023-02041-9
  24. Kristensen, N., Scoble, M. & Karsholt, O. (2007) Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity. In: Zhang, Z.-Q. & Shear, W.A. (Eds.), Linnaeus Tercentenary: progress in invertebrate taxonomy. Zootaxa, 1668, pp. 699–747. https://doi.org/10.11646/zootaxa.1668.1.30
  25. Lalonde, M.M.L. (2021) Phylogenetic analysis of the complete mitochondrial genome of the graphic beauty butterfly Baeotus beotus (Doubleday 1849) (Lepidoptera: Nymphalidae: Nymphalinae: Coeini), Mitochondrial DNA, Part B, 6 (4), 1516–1518. https://doi.org/10.1080/23802359.2021.1914526
  26. Llorente-Bousquets, J.E. & Castro-Gerardino, J. (2007) Estudios en sistemática de Dismorphiini (Lepidoptera: Pieridae) I. Morfología de huevos y su importancia taxonómica. Revista de la Academia Colombiana de Ciencias Físicas y Exactas, 31 (118), 145–164. https://doi.org/10.18257/raccefyn.31(118).2007.2323
  27. Llorente-Bousquets, J.E. & Castro-Gerardino, J. (2008) Morfología del corion en Dismorphiini (Lepidoptera: Pieridae). In: Llorente-Bousquets, J. & Lanteri, A. (Eds.), Contribuciones taxonómicas en órdenes de insectos hiperdiversos. Las Prensas de Ciencias, UNAM, México, D.F., pp. 72–90.
  28. Llorente-Bousquets, J., Nieves-Uribe, S., Flores-Gallardo, A., Hernández-Mejía, B.C. & Castro-Gerardino, J. (2018) Chorionic sculpture in the Dismorphiinae subfamily (Lepidoptera: Pieridae). Zootaxa, 4429 (2), 201–246. https://doi.org/10.11646/zootaxa.4429.2.1
  29. Llorente-Bousquets, J., Nieves-Uribe, S. & Flores-Gallardo, A. (2023) Exochorion in the tribe Nymphalini (Lepidoptera: Nymphalidae): the genus Hypanartia Hübner, [1821] and comparison with related genera. Zootaxa, 5530 (2), 151–200. https://doi.org/10.11646/zootaxa.5330.2.1
  30. Motta, P.C. (1989) Análise Filogenética de Ithomiinae (Lep.: Nymphalidae) com base nos ovos: relação com plantas hospedeiras. M.Sc. Thesis, SP: UNICAMP, Campinas, 294 pp.
  31. Müller, W. (1886) Südamerikanische Nymphalidenraupen: Versuch eines natürlichen Systems der Nymphaliden. Zoologische Jahrbücher, 1, 417–678. https://doi.org/10.5962/bhl.title.109410
  32. Muyshondt Jr., A. & Muyshondt, A. (1976) Notes on the life cycle and natural history of butterflies of El Salvador. I C. Colobura dirce L. (Nymphalidae-Coloburinae). Journal of the New York Entomological Society, 84, 23–33.
  33. Muyshondt, Jr. A. & Muyshondt, A. (1978) Notes on the life cycle and natural history of butterflies of El Salvador. II C. Smyrna blomfildia and S. karwinskii (Nymphalidae: Coloburini). Journal of the Lepidopterists’ Society, 32 (3), 160–174.
  34. Muyshondt Jr. A. & Muyshondt, A. (1979) Notes on the life cycle and natural history of butterflies of El Salvador. III C. Historis odius y Coea acheronta (Nymphalidae-Coloburinae). Journal of the Lepidopterists’ Society, 33 (2), 112–123.
  35. Nakanishi, A., Saigusa, T., Zhao, W.-Y. & Li, C.-L. (1997) Immature stages of Pseudregolis [sic] wedah (Kollar, 1844) (Lepidoptera, Nymphalidae). Nature and Human Activities, 2, 91–102.
  36. Nieves-Uribe, S., Flores-Gallardo, A., Hernández-Mejía, B.C. & Llorente-Bousquets, J. (2015) Exploración morfológica del corion en Biblidinae (Lepidoptera: Nymphalidae): aspectos filogenéticos y clasificatorios. Southwestern Entomologist, 40 (3), 589–648. https://doi.org/10.3958/059.040.0318
  37. Nieves-Uribe, S., Castro-Gerardino, J., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016a) Corion en los géneros Anteos y Rhabdodryas: su significado e implicaciones. Southwestern Entomologist, 41 (2), 485–504. https://doi.org/10.3958/059.041.0218
  38. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016b) Morfología coriónica de once especies de Biblidinae de México y Colombia: un examen de predicciones. Southwestern Entomologist, 41 (2), 505–532. https://doi.org/10.3958/059.041.0219
  39. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2017a) Corion de Ectima thecla thecla (Fabricius, 1796) y su comparación con el género Hamadryas. Southwestern Entomologist, 42 (3), 851–864. https://doi.org/10.3958/059.042.0324
  40. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2017b) Corion de Orophila cardases campaspe (Hewitson, 1869) y caracterización coriónica de la subtribu Callicorina. Southwestern Entomologist, 42 (3), 865–878. https://doi.org/10.3958/059.042.0325
  41. Nieves-Uribe, S., Flores-Gallardo, A., Llorente-Bousquets, J., Luis-Martínez, A. & Pozo, C. (2019) Use of exochorion characters for the systematics of Hamadryas Hübner and Ectima Doubleday (Nymphalidae: Biblidinae: Ageroniini). Zootaxa, 4619 (1), 77–108. https://doi.org/10.11646/zootaxa.4619.1.3
  42. Nieves-Uribe, S., Llorente-Bousquets, J. & Flores-Gallardo, A. (2021) Toward standards in practices and techniques on ootaxonomy in the Pieridae (Lepidoptera: Papilionidae). Zootaxa, 4985 (3), 301–344. https://doi.org/10.11646/zootaxa.4985.3.1
  43. Nieves-Uribe, S. & Llorente-Bousquets, J. (2022) Rehidratación abdominal con hidróxido de amonio en Lepidoptera: obtención del corion para estudios taxonómicos. Southwestern Entomologist, 47 (2), 481–498. https://doi.org/10.3958/059.047.0224
  44. Nylin, S. & Wahlberg, N. (2008) Does plasticity drive speciation? Host-plant shifts and diversification in Nymphalinae butterflies (Lepidoptera: Nymphalidae) during the Tertiary. Biological Journal of the Linnean Society, 94 (1), 115–130. https://doi.org/10.1111/j.1095-8312.2008.00964.x
  45. Oliveira-Neto, J.F, Dias, F.M.S., Pawoski, E., Oliveira, P., Casagrande, M.M. & Mielke, O.H.H. (2016) Immature stages of six species of Adelpha Hübner (Lepidoptera: Nymphalidae: Limenitidinae) from Southern Brazil Coastal Forests. Neotropical Entomology, 45, 524–536. https://doi.org/10.1007/s13744-016-0405-y
  46. Reuter, E. (1896) Über die palpen der Rhopaloceren, ein beitrag zur erkenntnis der verwandtschaftlichen beziehungen unter den tagfaltern. Acta Societatis Scientiarum Fennicae, 22 (1), 1–577. https://doi.org/10.5962/bhl.title.10329
  47. Rivera-Galicia, S., Nieves-Uribe, S. & Llorente-Bousquets, J. (2020) Estudio del exocorion en tres especies de Heliconiinae de México. Southwestern Entomologist, 45 (3), 753–779. https://doi.org/10.3958/059.045.0317
  48. Seitz, A. (1924) The Macrolepidoptera of the world: a systematic account of all the hitherto known Macrolepidoptera. Vol. 5. Fritz Lehmann Verlag, Stuttgart, 1139 pp. https://doi.org/10.5962/bhl.title.61923
  49. Scudder, S.H. (1893) The tropical fauna element of our Southern Nymphalinae systematically treated. Proceedings of the American Academy of Arts and Science, XXVII, 236–251. https://doi.org/10.2307/20020476
  50. Scudder, S.H. (1889) The butterflies of the eastern United States and Canada: with special reference to New. England in three volumes. Published by the author, Cambridge, 1958 pp. https://doi.org/10.5962/bhl.title.40436
  51. Shi, Q.-H., Sun, X.-Y., Wang, Y.-L., Hao, J.-S. & Yang, Q. (2015) Morphological characters are compatible with mitogenomic data in resolving the phylogeny of Nymphalid butterflies (Lepidoptera: Papilionoidea: Nymphalidae). PLoS ONE, 10 (4), e0124349, 1–19. https://doi.org/10.1371/journal.pone.0124349
  52. Sidal, M.E. & Whiting, M.F. (2005). Long-branch abstractions. Cladistics, 15 (1), 9–24. https://doi.org/10.1111/j.1096-0031.1999.tb00391.x
  53. Su, C., Shi, Q., Sun, X., Ma, J., Li, C., Hao, J. & Yang, Q. (2017) Dated phylogeny and dispersal history of the butterfly subfamily Nymphalinae (Lepidoptera: Nymphalidae). Scientific Reports, 7 (1), Art. 8799, 1–11. https://doi.org/10.1038/s41598-017-08993-w
  54. Suludere, Z. (1988a) Studies on the external morphology of the eggs of some Argynninae species (Satyridae: Lepidoptera). Communications of the Faculty of Sciences University of Ankara Series C Biology and Geological Engineering, 6, 9–28. https://doi.org/10.1501/Commuc_0000000125
  55. Suludere, Z. (1988b) Studies on the external morphology of the eggs of some Melitaea species (Satyridae: Lepidoptera). Communications of the Faculty of Sciences University of Ankara Series C Biology and Geological Engineering, 6, 73–84. https://doi.org/10.1501/Commuc_0000000129
  56. Van Son, G. (1979) The butterflies of Southern Africa. Part. IV Nymphalidae: Nymphalinae. The Transvaal Museum Memoir, 22 (1), 1–286. https://doi.org/10.10520/AJA0000012_253
  57. Wahlberg, N. (2006) Awkward age for butterflies: insights from the age of the butterfly subfamily Nymphalinae (Lepidoptera: Nymphalidae). Systematic Biology, 55 (5), 703–714. https://doi.org/10.1080/10635150600913235
  58. Wahlberg, N. (2019b) Nymphalinae. Nymphalidae.net, Wahlberg, N (Ed.). Available from: http://www.nymphalidae.net/Nymphalidae/General/Nymphalinae.htm (accessed 22 February 2024)
  59. Wahlberg, N., Brower, A.V.Z. & Nylin, S. (2005) Phylogenetic relationships and historical biogeography of tribes and genera in the subfamily Nymphalinae (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society, 86 (2), 227–251. https://doi.org/10.1111/j.1095-8312.2005.00531.x
  60. Wahlberg, N., Leneveu, J., Kodandaramaiah, U., Peña, C.A., Nylin, S., Freitas, A.V. & Brower, A.V. (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proceedings of the Royal Society B: Biological Sciences, 276, 4295–4302. https://doi.org/10.1098/rspb.2009.1303
  61. Wahlberg, N. & Nylin, S. (2003) Morphology versus molecules: resolution of the positions of Nymphalis, Polygonia, and related genera (Lepidoptera: Nymphalidae). Cladistics, 19 (3), 213–223. https://doi.org/10.1111/j.1096-0031.2003.tb00364.x
  62. Wahlberg, N., Weingartner, E. & Nylin, S. (2003) Towards a better understanding of the higher systematics of Nymphalidae (Lepidoptera: Papilionoidea). Molecular Phylogenetics and Evolution, 28 (3), 473–84. https://doi.org/10.1016/S1055-7903(03)00052-6
  63. Willmott, K.R. (2003) The genus Adelpha: its systematics, biology and biogeography (Lepidoptera: Nymphalidae: Limenitidini). Flora & Fauna Books, Gainesville, Florida, 322 pp.
  64. Willmott K.R., Constantino, M.L. & Hall, J.P.W. (2001) A review of Colobura (Lepidoptera: Nymphalidae) with comments on larval and adult ecology and description of a sibling species. Annuals of the Entomological Society of America, 94 (2), 185–196. https://doi.org/10.1603/0013-8746(2001)094[0185:AROCLN]2.0.CO;2
  65. Wu, Z.-Y., Provan, J., Wang, H., Chen, C.-J., Cadotte, M.W., Luo, Y.-H., Amorim, B.S., Li, D.-Z. & Milne, R.I. (2018) Testing Darwin’s transoceanic dispersal hypothesis for the inland nettle family (Urticaceae). Ecology Letters, 21 (10), 1515–1529. https://doi.org/10.1111/ele.13132
  66. Zhang, M., Zhong, Y., Cao, T., Geng, Y., Zhang, Y., Jin, K., Ren, Z., Zhang, R., Guo, Y. & Ma, E. (2008) Phylogenetic relationships and morphological evolution in the subfamily Limenitidinae (Lepidoptera: Nymphalidae). Progress in Natural Science, 18, 1357–1364. https://doi.org/10.1016/j.pnsc.2008.03.025
  67. Zhang, J., Cong, Q., Shen, J., Opler, P.A. & Grishin, N.V. (2021) Genomics-guided refinement of butterfly taxonomy. The Taxonomic Report of the International Lepidoptera Survey, 9 (3), 1–55. https://doi.org/10.5281/zenodo.5630311