Abstract
Using scanning electron microscopy (SEM), we examine and compare the micropylar and perimicropylar regions of the egg exochorion in six genera of the subfamily Dismorphiinae (Pieridae): Leptidea Billberg, Enantia Hübner, Pseudopieris Godman & Salvin, Lieinix Gray, Dismorphia Hübner, and Moschoneura Butler. We provide the first descriptions of the morphological structures of the chorion in these genera. Leptidea is the most primitive genus, and Dismorphia represents the most diverse. We examined the jethys complex of Enantia to study diversity of characters within the genus. We conclude that the exochorion of Dismorphiinae is the most plesiomorphic in relation to Coliadinae and Pierinae, owing to its simple morphology without a transition zone surrounding the wreath (perimicropylar region). Leptidea (Leptideini) shows the least derived characters of the subfamily, followed by Enantia (Dismorphiini). The latter genus exhibits several typical characters of the tribe that are distinctive from other more specialized genera. Exochorionic similarities among the four species of the jethys complex support their close relationship; E. mazai exhibits the most derived features among the species of the complex. Pseudopieris and Moschoneura exhibit several plesiomorphies, such as a large number of openings (micro-grid), but they also show some derived features, such as three semi-rings in the wreath. Dismorphia and Lieinix exhibit characters in their most derived states, such as a striated micro-grid (most conspicuous in Lieinix) and basal aeropyles (most conspicuous in Dismorphia), a character shared with Moschoneura. The purpose of this work is exploratory and descriptive and would be improved by a larger sample size. This contribution is the third in a series of studies on the chorion of Dismorphiinae eggs.
References
Acosta-Fernández, B. (2008) Una nueva subespecie de Euchloe belemia (Esper, [1800]) de la isla de Gran Canaria, Islas Canarias, España (Lepidoptera: Pieridae). SHILAP Revista de Lepidopterología, 36 (142), 173–182.
Back, W. (1984) Beschreibung der präimaginalstaiden von Euchloe tagis pechi Straudinger, 1885 (Lep., Pieridae). Atalanta, 15 (1/2), 152–164.
Back, W. (1990) Taxonomische untersuchungen innerhalb der antengruppe um Euchloe ausonia (Hübner, 1804) (Lepidoptera, Pieridae). Atalanta, 21 (3/4), 187–206.
Braby, M.F. & Nishida, K. (2007) The immature stages, larval food plants and biology of Neotropical mistletoe butterflies. I. The Hesperocharis group (Pieridae: Anthocharidini). Journal of the Lepidopterists’ Society, 61 (4), 181–195.
https://doi.org/10.1080/00222931003633227
Braby, M.F., Pierce, N.E. & Vila, R. (2007) Phylogeny and historical biogeography of the subtribe Aporiina (Lepidoptera: Pieridae): implications for the origin of Australian butterflies. Biological Journal of the Linnean Society, 90 (3), 413–440.
https://doi.org/10.1111/j.1095-8312.2007.00732.x
Butler, A.G. (1870) A revision of the genera of the subfamily Pierinae. Cistula Entomologica, 1 (3), 33–58.
Castro-Gerardino, D.J. & Llorente-Bousquets, J. (2017) Comparative exploration of antennae in Pseudopontia, and antennal clubs of the tribes Leptideini and Dismorphiini (Lepidoptera: Pieridae). Zootaxa, 4347 (3), 401–445.
https://doi.org/10.11646/zootaxa.4347.3.1
Castro-Gerardino, D.J. & Llorente-Bousquets, J. (2019) Antennal ultrastructure in Patia (Pieridae, Dismorphiinae). Zootaxa, 4559 (3), 445–472
https://doi.org/10.11646/zootaxa.4559.3.2
Cheong, S.W., Lee, C.E. & Park, H.C. (1990) A microscopic study on the bursa copulatrix of Korean Pieridae (Lepidoptera). Esakia, 1, 167–172.
Cheong, S.W. & Lee, C.E. (1992) Comparative morphology and phylogeny on female internal genitalia of the Pieridae (Lepidoptera). Metamorphosis, 3 (4), 139–147.
Dickson, C.G.C. & Kroon, D.K. (Eds.) (1978) Pennington’s Butterflies of Southern Africa. 1st Edition. Ad. Donker. Johannesburg, 800 pp.
Dolinskaya, I.V. (2019) The use of egg characters for the classification of Notodontidae (Lepidoptera), with keys to the common Paleartic genera and species. Zootaxa, 4604 (2), 201–241.
https://doi.org/10.11646/zootaxa.4604.2.1
Döring, E.K.H. (1955) Zur Morphologie der Schmetterlingseier. Akademie-Verlag, Berlin, 154 pp., 61 pls.
Ehrlich, P.R. (1958) The comparative morphology, phylogeny and higher classification of the butterflies (Lepidoptera: Papilionoidea). The University of Kansas Science Bulletin, 39 (8), 305–370.
Fitzhugh, K. (2006) The abduction of phylogenetic hypothesis. Zootaxa, 1145 (1), 1–110.
https://doi.org/10.11646/zootaxa.1145.1.1
Grote, A.R. (1900) The descent of the pierids. Proceedings of the American Philosophical Society, 39 (161), 4–67.
Häuser, C.L. (1993) Die inneren 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.
Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets, J. (2013) Comparación morfológica del corion de especies de los géneros Pieriballia, Itaballia y Perrhybris (Lepidoptera: Pieridae: Pierinae), y sus implicaciones filogenéticas. Southwestern Entomologist, 38 (2), 275–292.
https://doi.org/10.3958/059.038.0211
Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets, J. (2014a) Morfología del corion en especies de los géneros Ascia y Ganyra y su comparación con otros géneros próximos de Pierinae (Lepidoptera: Pieridae). Southwestern Entomologist, 39 (1), 119–134.
https://doi.org/10.3958/059.039.0112
Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets, J. (2014b) Morfología del corion en la subfamilia Coliadinae (Lepidoptera: Pieridae). Southwestern Entomologist, 39 (4), 853–886.
https://doi.org/10.3958/059.039.0416
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
Hernández-Roldán, J.L., Munguira, M.L., Wagner, W. & Vila, R. (2012) Comparative analysis and taxonomic use of the morphology of immature stages and natural history traits in European species of Pyrgus Hübner (Lepidoptera: Hesperiidae, Pyrginae). Zootaxa, 3470 (1), 1–71. [monograph]
https://doi.org/10.11646/zootaxa.3470.1.1
Higgins, L.G. (1975) The classification of European butterflies. Collins, London, 320 pp.
Igarashi, S. & Fukuda, H. (2000) The life histories of Asian butterflies. Vol. 2. Tokai University Press, Tokyo, 711 pp., 425 color pls.
Jordan, K. (1898) Contributions to the Morphology of Lepidoptera. Novitates Zoologicae, 5, 374–415.
https://doi.org/10.5962/bhl.part.1650
Kaminski, L.A., Barbosa, E.P. & Freitas, A.V.L. (2012) Immature stages of the Neotropical mistletoe butterfly Cunizza hirlanda planasia Fruhstorfer (Pieridae: Anthocharidini). Journal of the Lepidopterists’ Society, 66 (3), 143–146.
https://doi.org/10.18473/lepi.v66i3.a4
Kaminski, L.A., Tavares, M., Ferro, V.G. & Moreira G.R.P. (2002) Morfologia externa dos estágios imaturos de heliconíneos neotropicais. III. Heliconius erato phyllis (Fabricius) (Lepidoptera, Nymphalidae, Heliconiinae). Revista Brasileira de Zoologia, 19 (4), 993–993.
https://doi.org/10.18473/lepi.v66i3.a4
Klots, A.B. (1931–1933) A generic classification of the Pieridae (Lepidoptera) together with a study of the male genitalia. Entomologica Americana, 12, 139–242.
Lamas, G. (1979) Los Dismorphiinae (Pieridae) de México, América Central, y las Antillas. Revista de la Sociedad Mexicana de Lepidopterología, 5 (1), 3–37.
Lamas, G. (2004) Twenty-five new Neotropical Dismorphiinae (Lepidoptera-Pieridae). Revista Peruana de Entomología, 44, 17–36.
Llorente–Bousquets, J. (1984) Sinopsis sistemática y biogeográfica de los Dismorphiinae de México con especial referencia al género Enantia Hübner (Lepidoptera: Pieridae). Folia Entomológica Mexicana, 58, 3–206.
Llorente-Bousquets, J. & Castro-Gerardino, J. (2004) Subfamilia Dismorphiinae. In: LeCrom, J.F., Llorente-Bousquets, J., Constantino, L.M. & Salazar, J.A. (Eds.), Mariposas de Colombia. Tomo 2. Pieridae. Carlec, Bogotá, pp. 14–15.
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.
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 City, pp. 72–90.
Llorente-Bousquets, J. & Castro-Gerardino, D.J. (2018) Antennal ultrastructure of Leptidea Billberg, 1820 (Pieridae: Dismorphiinae: Leptideini) and its taxonomic implications. Zootaxa, 4402 (3), 401–442.
https://doi.org/10.11646/zootaxa.4402.3.1
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
Mazel, R. (2005) Élements de phylogénie dans le genre Leptidea Bilberg 1820 (Lepidoptera, Pieridae, Dismorphiinae). Revue de l’Association Roussillonnaise d’Entomologie, 14, (3), 98–111.
Munguira, M.L., Martín, J., García-Barros, E., Shahbazian, G. & Cancela, J.P. (2015) Morphology and morphometry of Lycaenid eggs (Lepidoptera: Lycaenidae). Zootaxa, 3937 (2), 201–247.
https://doi.org/10.11646/zootaxa.3937.2.1
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
Nieves-Uribe, S., Castro-Gerardino, J., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016b) Microrretícula coriónica en los géneros Nathalis Boisduval y Kricogonia Reakirt: implicaciones taxonómicas y tendencias evolutivas. Southwestern Entomologist, 41 (3), 716–733.
https://doi.org/10.3958/059.041.0314
Nieves-Uribe, S., Castro-Gerardino, J. Flores-Gallardo, A. & Llorente-Bousquets, J. (2016c) Estudio del corion de tres especies del género Colias Fabricius, 1807 y Zerene cesonia cesonia (Stoll, 1790). Southwestern Entomologist, 41 (4), 1121–1141.
https://doi.org/10.3958/059.041.0411
Nieves-Uribe, S. Flores-Gallardo, A. & Llorente-Bousquets, J. (2018a) Corion de Leucidia brephos (Hübner, [1809]), comparaciones con otros géneros de Coliadinae y tendencias reticulares. Southwestern Entomologist, 43 (1), 239–255.
https://doi.org/10.3958/059.043.0115
Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2018b) Estructura exocoriónica en tres especies de Colias Fabricius, 1807 (Lepidoptera: Pieridae, Coliadinae). Southwestern Entomologist, 43 (2), 485–503.
https://doi.org/10.3958/059.043.0220
Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2020) Chorion exploration in the tribe Anthocharidini (Lepidoptera: Pieridae) and their possible importance in its systematics. Zootaxa, 4868 (2), 151–207.
https://doi.org/10.11646/zootaxa.4868.2.1
Reuter, E. (1898) On a new classification of the Rhopalocera. Entomologist’s Record and Journal of Variation, 10 (2), 25–26.
Schatz, E. (1885–1888) II. Theil. Die Familien und Gattungen der Taglater systematisch un analytisch bearbeitet. In: Staudinger, O. & Schatz, E. (Eds.), 1884–1892, Exotische schmetterlinge. Fürth von G. Löwensohn, Bayern, pp. 1–34.
Staudinger, O. (1884–1888) I. Theil. Exotische tagfalter in systematischer reiherfolge mit betücksichtigung neuer arte. In: Staudinger, O. & Schatz, E. (Eds.), 1884–1892, Exotische schmetterlinge. Fürth von G. Löwensohn, Bayern, pp. 1–33.
https://doi.org/10.5962/bhl.title.60853
Vane-Wright, R.I. (2003) Evidence and identity in butterfly systematics. In: Boggs, C.L., Watt, W.B. & Ehrlich, P.R. (Eds.), Butterflies, ecology, and evolution taking flight. The University of Chicago Press, Chicago, Illinois, pp. 477–513.
Wahlberg N., Rota, J., Braby, M.F., Pierce, N.E. & Wheat, C.W. (2014) Revised Systematics and higher classification of pierid butterflies (Lepidoptera: Pieridae) based on molecular data. Zoological Script, 43 (6), 641–650.
https://doi.org/10.1111/zsc.12075
Yata, O. (1981) Comparative morphology of the pupal forewing tracheation in some Japanese species of the family Pieridae (Lepidoptera). Kontyû, 49 (2), 245–257.