Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2017-11-14
Page range: 401–445
Abstract views: 99
PDF downloaded: 6

Comparative exploration of antennae in Pseudopontia, and antennal clubs of the tribes Leptideini and Dismorphiini (Lepidoptera: Pieridae)

Smithsonian Institution, PO Box 37012, Washington, DC. 20013–7012 USA. Museo de Zoología, Depto. Biología Evolutiva Fac. Ciencias. UNAM.
Smithsonian Institution, PO Box 37012, Washington, DC. 20013–7012 USA. Museo de Zoología, Depto. Biología Evolutiva Fac. Ciencias. UNAM.

Abstract

We examined antennal ultrastructure in species of Dismorphiinae and Pseudopontiinae (Pieridae) using scanning electron microscopy (SEM). We examined two species of Pseudopontia (Pseudopontiinae) and more than 30 species in seven genera of two tribes in the subfamily Dismorphiinae: Leptidea, Enantia, Pseudopieris, Lieinix, Moschoneura, Dismorphia, and Patia. We focused on the scaleless terminal area of the antenna where there are many types of sensilla, some of which are clustered together and constitute specialized organs. We measured, described, and illustrate at different magnifications structures including the antennal club, antennomeres, sulci, pseudosulci, and chaetic, trichoid, coeloconic, basiconic, and auriculate sensilla, as well as other previously unnamed sensilla. From these antennal features, we created a matrix of characters that allowed us to recognize divergence between the tribes Leptideini and Dismorphiini. The antennae of Leptideini have fewer scaleless antennomeres in the antennal club than those of Dismorphiini, a greater number of pseudosulci disaggregated or dispersed (in Leptidea), and fewer types of sensilla and microtrichia (a more homogeneous antennal morphology), as well as a reduction in the density of sensilla. In Leptidea the antennal form is more specialized: it is shorter in comparison to genera of other Papilionoidea families. We also created a matrix of general morphological characters of Dismorphiinae and Pieridae from the taxonomic literature. This matrix confirms the marked character divergence between the tribes and allows for a more meaningful discussion regarding the relationships between Dismorphiinae and the other subfamilies of Pieridae (i.e., Pseudopontiinae, Coliadinae, and Pierinae). We argue that Pseudopontiinae cannot be considered the least derived subfamily among Pieridae because pupal features, wing venation, and antennal characters exhibit a combination of primitive and specialized states. In addition, we discuss our results from the perspective of patterns of food plant usage in pierid subfamilies, specifically the diversification of several Dismorphiinae genera on Hologalegina and Ingeae (Fabaceae).

 

References

  1. Allan, G.J. & Porter, J.M. (2000) Tribal delimitation and phylogenetic relationships of Loteae and Coronilleae (Faboideae: Fabaceae). American Journal of Botany, 87 (12), 1871–1881.
    https://doi.org/10.2307/2656839

    Asmussen, C.B. & Liston, A. (1998) Chloroplast DNA characters, phylogeny, and classification of Lathyrus (Fabaceae). American Journal of Botany, 85 (3), 387–401.
    https://doi.org/10.2307/2446332

    Awata, H., Wakakuwa, M. & Arikawa, K. (2009) Evolution of color in Pierid butterflies: blue opsin duplication, ommatidial heterogeneity and eye regionalization in Colias erate. Journal of Comparative Physiology A, 195 (4), 401–408.
    https://doi.org/10.1007/s00359-009-0418-7

    Beccaloni, G.W., Viloria, A., Hall, S.K. & Robinson, G.S. (2008) Catalogue of the hostplants of the Neotropical butterflies. Monografias Tercer Milenio N°8. Sociedad Entomológica Aragonesa & Red Iberoamericana de Biogeografía y Entomología Sistemática, Zaragoza, 534 pp.

    Bell, C.D., Soltis, D.E. & Soltis, P.S. (2010) The age and diversification of the angiosperms re-revisited. American Journal of Botany, 97 (8), 1296–1303.
    https://doi.org/10.3732/ajb.0900346

    Belló, M.A., Rudall, P.J. & Hawkins, J.A. (2012) Combined phylogenetic analyses reveal interfamilial relationships and patterns of floral evolution in the eudicot order Fabales. Cladistics, 28 (4), 393–421.
    https://doi.org/10.1111/j.1096-0031.2012.00392.x

    Bodine, D. (1896) The Taxonomic Value of the Antennae of the Lepidoptera. A Thesis Presented to the Faculty of Cornell University May 1, 1895, for the Degree of Doctor of Science. Transactions of the American Entomological Society, 23 (1), 1–61.

    Braby, M.F. & Trueman, J.W.H. (2006) Evolution of larval host plant associations and adaptive radiation in pierid butterflies. Journal of Evolutionary Biology, 19 (5), 1677–1690.
    https://doi.org/10.1111/j.1420-9101.2006.01109.x

    Braby, M.F., Vila, R. & Pierce, N.E. (2006) Molecular phylogeny and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zoological Journal of the Linnean Society, 147 (2), 239–275.
    https://doi.org/10.1111/j.1096-3642.2006.00218.x

    Brown, G.K. (2008) Systematics of the tribe Ingeae (Leguminosae-Mimosoideae) over the past 25 years. Muelleria, 26 (1), 27–42.

    Brown, G.K., Murphey, D.J., Miller, J.T. & Ladiges, P.Y. (2008) Acacia s.s. and its relationships among tropical legumes, Tribe Ingeae (Leguminosae: Mimosoidea). Systematic Botany, 33 (4), 739–751.
    https://doi.org/10.1600/036364408786500136

    Butler, A.G. (1870) A revision of the genera of the sub-family Pierinae Cistula Entomologica, 1 (3), 33–58.

    Cheong, S.W., Lee, C.E. & Park, H.C. (1990) A microscopic study on the bursa copulatrix of Korean Pieridae (Lepidoptera). Esakia, Special Issue, 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.

    Clench, H.K. (1955) Revised classification of the butterfly family Lycaenidae and its allies. Annals of the Carnegie Museum, 33, 261–274.

    de Jong, R. & Van Achterberg, C. (2007) Global disjunctions and flying insects. In: Renema, W. (Ed.), Biogeography, Time, and Place: Distributions, Barriers, and Islands. Springer, Dordrecht, pp. 5–44.
    https://doi.org/10.1007/978-1-4020-6374-9_1

    de Lesse H. (1967) Les nombres de chromosomes chez les Lépidoptères Rhopalocères néotropicaux. Annales de la Société entomologique de France, New Sereis, 67–136.

    Dias, F.M.S., Leviski, G.L., Casagrande, M.M. & Mielke O.H.H. (2016) Dismorphia melia Godart [1824] (Pieridae: Dismorphiinae): external morphology of the last instar and pupa, with notes on its taxonomy, variation, and distribution. The Journal of the Lepidopterists’ Society, 70 (1), 61–71.
    https://doi.org/10.18473/lepi.70i1.a7

    Ding, C. & Zhang, Y. (2017) Phylogenetic relationships of Pieridae (Lepidoptera: Papilionoidea) in China based on seven gene fragments. Entomological Science, 20 (1), 15–23.
    https://doi.org/10.1111/ens.12214

    Downey, J.C. & Allyn, A.C. (1975) Wing-scale morphology and nomenclature. Bulletin of the Allyn Museum, 31, 1–32.

    Doyle, J.J. & Luckow, M.A. (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiology, 131 (3), 900–910.
    https://doi.org/10.1104/pp.102.018150

    Ehrlich, P. (1958) The comparatice morphology, phylogeny, and higher classification of the butterflies (Lepidoptera: Papilionoidea). University of Kansas Science Bulletin, 39, 305–370.

    Ghiradella, H. (1998) Hairs, bristles, and scales. In: Harrison, F.W. & Locke, M. (Ed.), Microscopic Anatomy of Invertebrates. Vol. 11A. Insecta. Wiley-Liss, New York, pp. 257–287.

    Godman, F.D. & Salvin, O. (1879–1901) Insecta. Lepidoptera-Rhopalocera. Biologia Centrali-Americana. Vol II. Taylor and Francis, London, 782 pp.

    Grehan, J.R. (1991) A panbiogeographic for pre-cretaceous Angiosperm-Lepidoptera coevolution. Australian Systematic Botany, 4 (1), 91–110.
    https://doi.org/10.1071/SB9910091

    Grimes, J. (1999) Inflorescense morphology, heterochrony, and phylogeny in the mimosoid tribes Ingeae and Acacieae (Leguminosae: Mimosoideae). The Botanical Review, 65 (4), 317–347.
    https://doi.org/10.1007/BF02857753

    Grote, R. (1900) The descent of the pierids. Proceedings of the American Philosophical Society, 39 (161), 4–67.

    Hallberg, E., Löfstedt, C. & Hansson, B.S. (2003) Sensilla and proprioceptors. In: Kristensen, N.P. (Ed.), Handbook of Zoology: Lepidoptera, Moths and Butterflies: Vol 2 Morphology, Physiology and Development. De Gruyter, Berlin, pp. 267–288

    Häuser, C.L. (1993) Die inneren weiblichen Genitalorgane der Tagfalter (Rhopalocera): Vergleichende Morphologie und phylogenetische Interpretation (Insecta, Lepidoptera). [The internal female genital organ in butterflies (Rhopalocera): comparative morphology and phylogenetic intepretation (Insecta, Lepidoptera)]. Zoologische-Jahrbucher, Abeteilung fur-Systematik, Okologie und-Geographie-Tiere, 120 (4), 389–439.

    Heikkilä, M., Kaila, L., Mutanen, M., Peña, C. & Wahlberg, N. (2012) Cretaceous origin and repeated tertiary diversification of the redefined butterflies. Proceedings of the Royal Society B: Biological Sciences, 279 (1731), 1093–1099.
    https://doi.org/10.1098/rspb.2011.1430

    Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets J. (2013) Comparación morfológica del corion de especies de los géneros Pieriballia, Itabalia 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, B.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

    Higgins, L.G. (1975) The classification of European butterflies. Collins, London, 320 pp.

    Jong de, R., Vane-Wright, R.I. & Ackery, P.R. (1996) The higher classification of butterflies (Lepidoptera): problems and prospects. Entomologica Scandinavica, 27 (1), 65–101.
    https://doi.org/10.1163/187631296X00205

    Jordan, K. (1898) Contributions to the Morphology of Lepidoptera. Novitates Zoologicae, 5, 374–415.

    Keil, T.A. (1999) Morphology and development of the peripheral olfactory organs. In: Hansson, B.S. (Ed.), Insect olfaction. Springer, Berlin/Heidelberg, pp. 5–47
    https://doi.org/10.1007/978-3-662-07911-9_2

    Klots, A.B. (1931–1933) A generic revision of the Pieridae (Lepidoptera), together with a study of the male genitalia. Entomologica Americana, 12 (3), 139–242.

    Lamas, G. (1979) Los Dismorphiinae (Pieridae) de Mexico, America 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 (1), 17–36.

    Li-zhong, H. (2005) List of chinese insects. Vol. III. Sun Yat-sen University Press & Guangwei Printers, Guangzhou, 595 pp.

    Llorente, J. (1984) Sinopsis Sistemática y Biogeográfica de los Dismorphiinae de México con especial referencia al género Enantia Huebner (Lepidoptera: Pieridae). Folia Entomologica Mexicana, 58, 1–207.

    Llorente-Bousquets, J. & Castro-Gerardino J. (2004) Subfamilia Dismorphiinae. In: LeCrom, J.F., Constantino, L.M., Llorente-Bousquets, J. & Salazar, J.A. (Eds.), Mariposas de Colombia Tomo 2. Pieridae. Ed. Carlec, Bogotá, pp. 14–16

    Llorente-Bousquets, J. & 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 Exactas, Físicas y Naturales, 31 (118), 145–164.

    Llorente-Bousquets, J. & 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. 71–90

    Lorkovič, Z. (1993) Leptidea reali Reissinger, 1989 (= lorkovicii Réal 1988), a new European species (Lepid., Pieridae). Natura Croatica, 2 (1), 1–26.

    Luckow, M., Miller, J.T., Murphy, D.J. & Livshultz, T. (2003) A phylogenetic analysis of the Mimosoideae (Leguminosae) based on chloroplast DNA sequence data. In: Klitgaard, B.B. & Bruneau, A. (Eds.), Advances in Legume Systematics, part 10, Higher Level Systematics. Royal Botanic Gardens, Kew, pp. 197–220

    Lukhtanov, V.A., Dincă, V., Talavera, G. & Vila, R. (2011) Unprecedented within-species chromosome number cline in the Wood White butterfly Leptidea sinapis and its significance for karyotype evolution and speciation. BMC Evolutionary Biology, 11 (1), 109.
    https://doi.org/10.1186/1471-2148-11-109

    Magallón, S. (2009) Flowering plants (Magnoliophyta). In: Hedges, S.B. & Kumar, S. (Eds.), The timetree of life. Oxford University Press, Oxford, pp. 161–165.

    Magallón, S. (2010) Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology, 59 (4), 384–399.
    https://doi.org/10.1093/sysbio/syq027

    Magallón, S. (2014) A review of the effect of relaxed clock method, long branches, genes, and calibrations in the estimation of angiosperm age. Botanical Sciences, 92 (1), 1–22.
    https://doi.org/10.17129/botsci.37

    Magallón, S. & Castillo, A. (2009) Angiosperm diversification through time. American Journal of Botany, 96 (1), 349–365.
    https://doi.org/10.3732/ajb.0800060

    Magallón, S., Gómez-Acevedo, S., Sánchez‐Reyes, L.L. & Hernández-Hernández, T. (2015) A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist, 207 (2), 437–453.
    https://doi.org/10.1111/nph.13264

    Maslin, B.R., Miller, J.T. & Seigler, D.S. (2003) Overview of the generic status of Acacia (Leguminoseae: Mimosoideae). Australian Systematic Botany, 16 (1), 1–18.
    https://doi.org/10.1071/SB02008

    Mazel, R. (2005) Éléments de phylogénie dans le genre Leptidea Bilberg 1820 (Lepidoptera, Pieridae, Dismorphiinae). Revue l’Association Roussillonaise d’Entomologie, 14 (3), 98–111.

    Miller, J.T. & Bayer, R.J. (2001) Molecular phylogenetics of Acacia (Fabaceae: Mimosoideae) based on the chloroplast matK coding sequence and flanking trnK intron spacer regions. American Journal of Botany, 88 (4), 697–705.
    https://doi.org/10.2307/2657071

    Miller, J.T., Murphy, D.J., Brown, G.K., Richardson, D.M. & González Orozco, C.E. (2011) The evolution and phylogenetic placement of invasive Australian Acacia species. Diversity and Distributions, 17 (5), 848–860.
    https://doi.org/10.1111/j.1472-4642.2011.00780.x

    Mitter, K.T., Larsen, T.B., De Prins, W., De Prins, J., Collins, S., Vande Weghe, G., Sáfián, Sz., Zakharov, E.V., Hawthorne, D.J., Kawahara, A.Y. & Regier J.C. (2011) The butterfly subfamily Pseudopontiinae is not monobasic: marked genetic diversity and morphology reveal three new species of Pseudopontia (Lepidoptera: Pieridae). Systematic Entomology, 36 (1), 139–163.
    https://doi.org/10.1111/j.1365-3113.2010.00549.x

    Nieves-Uribe, S., Castro-Gerardino, J., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016a) Corion en los géneros Anteos y Rhabdodryas (Pieridae: Coliadinae): 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 Krikogonia Reakirt (Lepidoptera: Pieridae): implicaciones taxonómicas y tendencias evolutivas. Southwestern Entomologist, 41 (3), 715–734.
    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

    Papageorgis, C. (1975) Mimicry in neotropical butterflies. American Scientist, 63 (5), 522–532.

    Reuter, E. (1896) Ueber die Palpen der Rhopaloceren. Ein Bei-trag zur Erkenntniss der verwandtschaftlichen Beziehungen unter den Tagfaltern. Acta Societatia Scientiarum Fennicae, 22 (1), 1–577.

    Reuter, E. (1898) On a new classification of the Rhopalocera. Entomologist’s Record and Journal of Variation, West Wickham, 10 (2), 25–26.

    Robbins, R.K. (1989) Systematic implications of butterfly leg structures that clean the antennae. Psyche, 96 (3–4), 209–222.
    https://doi.org/10.1155/1989/43420

    Robinson, G.S., Ackery, P.R., Kitching, I.J., Beccaloni, G.W. & Hernández, L.M. (2010) HOSTS―a Database of the World’s Lepidopteran Hostplants. Natural History Museum, London. Available from: http://www.nhm.ac.uk/research-curation/projects/hostplants/ (accessed 4 June 2017)

    Rodrigues de Souza, E., Lewis, G.P., Forest, F., Schnadelbach, A.S., van den Berg, C. & de Queiroz, L.P. (2013) Phylogeny of Calliandra (Leguminosae: Mimosoideae) based on nuclear and plastid molecular markers. Taxon, 62 (6), 1200–1219.
    https://doi.org/10.12705/626.2

    Rutowski, R.L., Macedonia, J.M., Kemp, D.J. & Taylor-Taft, L. (2007) Diversity in structural ultraviolet coloration among female sulphur butterflies (Coliadinae, Pieridae). Arthropod Structure & Development, 36 (3), 280–290.
    https://doi.org/10.1016/j.asd.2006.11.005

    Sáfián, Sz. (2015) Behaviour and development of Pseudopontia gola Sáfián & Mitter, 2011 (Lepidoptera: Pieridae). SHILAP, Revista de Lepidopterología, 43 (169), 85–89.

    Saura, A., Von Schoultz, B., Saura, A.O. & Brown, K.S. (2013) Chromosome evolution in Neotropical butterflies. Hereditas, 150 (2–3), 26–37.
    https://doi.org/10.1111/j.1601-5223.2013.00008.x

    Schenk, O. (1903) Die antennalen Hautsinnesorgane einiger Lepidopteren und Hymenopteren. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere, 17, 573–618.
    https://doi.org/10.5962/bhl.part.4636

    Scott, J.A. (1984) The phylogeny of butterflies (Papilionoidea and Hesperioidea). Journal of Research on the Lepidoptera, 23 (4), 241–281.

    Sellier, R. (1974) Donnees documentaires sur l'ultrastructure des recepteurs sensoriels antennaires chez les Lepidopteres rhopaloceres; etude en microscopie electronique par balayage. Annales de la Societe Entomologique de France, 10, 917–937.

    Shields, V.D.C. & Hildebrand, J.G. (1999a) Fine structure of antennal sensilla of the female sphinx moth, Manduca sexta (Lepidoptera: Sphingidae). I. Trichoid and basiconic sensilla. Canadian Journal of Zoology, 77 (2), 290–301.
    https://doi.org/10.1139/z98-204

    Shields, V.D.C. & Hildebrand, J.G. (1999b) Fine structure of antennal sensilla of the female sphinx moth, Manduca sexta (Lepidoptera: Sphingidae). II. Auriculate, coeloconic, and styliform complex sensilla. Canadian Journal of Zoology, 77 (2), 302–313.
    https://doi.org/10.1139/z99-003

    Shields, V.D.C. (2008) Ultrastructure of insect sensilla. In: Capinera, J.L. (Ed.), Encyclopedia of Entomology. Springer, Dordrecht, pp. 4009–4023.
    https://doi.org/10.1007/978-1-4020-6359-6_2295

    Šíchová, J., Voleniková, A., Dincă, V., Nguyen, P., Vila, R., Sahara, K. & Marec, F. (2015) Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies. BMC Evolutionary Biology, 15 (1), 1–16.
    https://doi.org/10.1186/s12862-015-0375-4

    Stavenga, D.G. & Arikawa, K. (2006) Evolution of color and vision of butterflies. Arthropod, Structure & Development, 35 (4), 307–318.
    https://doi.org/10.1016/j.asd.2006.08.011

    Steele, K.P. & Wojciechowski, M.F. (2003) Phylogenteic analyses of tribes Trifolieae and Vicieae, based on sequences of the plastid gene matK (Papilionoideae: Leguminosae). In: Klitgaard, B.B. & Bruneau, A. (Eds.), Advances in Legume Systematics. Part 10. Higher Level Systematics. Royal Botanic Gardens, Kew, pp. 355–370.

    Steinbrecht, R.A. (1999) Olfactory receptors. In: Eguchi, E. & Tominaga, Y. (Eds.), Atlas of Arthropod Sensory Receptors, Dynamic Morphology in Relation to Function. Springer-Verlag, Tokyo, pp. 155–176.

    Tennent, W.J. (1993) A critical note on the occurrence of Leptidea Billberg, 1820 species in North-West Africa (Lepidoptera: Pieridae). Phegea, 21 (4), 109–112.

    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, pp. 477–513

    Vázquez Nin, G. & Echeverría, O. (2000) Introducción a la Microscopía Electrónica Aplicada a las Ciencias Biológicas. Fondo de Cultura Económica, Mexico City, 168 pp.

    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. Zoologica Scripta, 43 (6), 641–650.
    https://doi.org/10.1111/zsc.12075

    Winhard, W. (1996) Convergent development of color patterns in butterflies: Field studies in Asia, Africa and South America. Spixiana, 21 (Supplement), 1–192.

    Winhard, W. (2016) Was macht Schmetterlinge ähnlich, wenn nicht verwandtschaft? Erläutert an Beispielen aus Südamerika, hauptsächtlich Kolumbien und Ecuador mit Neubeschreibungen einer Art und von 17 Unterarten (Lepidoptera, Pieridae, Nymphalidae). Atalanta, 47 (3/4), 290–319.

    Wojciechowski, M.F., Sanderson, M.J., Steele, K.P. & Liston, A. (2000) Molecular phylogeny of the ‘Temperate’ herbaceous tribes of Papilionid legumes: a super tree approach. In: Herendeen, P.S. & Bruneau, A. (Eds.), Advances in Legume Systematics. Vol. 9. Royal Botanic Gardens, Kew, pp. 277–298

    Wojciechowski, M.F. (2003) Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perspective. In: Klitgaard, B.B. & Bruneau, A. (Eds.), Advances in Legume Systematics. Part 10. Higher level systematics. Royal Botanic Gardens, Kew, pp. 5–35.

    Yoshimoto, H. (2000) Wood whites (Pieridae), the most primitive pierids? Butterflies, 26, 52–59.