Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2025-05-15
Page range: 1-34
Abstract views: 181
PDF downloaded: 20

Integrative taxonomy, phylogeny and distribution patterns of the diverse Neotropical cloud forest butterfly genus Perisama Doubleday (Nymphalidae, Biblidinae, Callicorini)

Nature Education Centre; Jagiellonian University; Gronostajowa 5; 30-387 Kraków; Poland
Department of Biology; Lund University; Solvegatan 35; Lund 223 62; Sweden
7 Lotissement l’Horizon; Le Puy Sainte Réparade; France
Programa Académico de Biología; Facultad de Ciencias Naturales y Matemáticas; Universidad Distrital Francisco José de Caldas; Carrera 10 N° 19-62; Bogota; Colombia.
Programa Académico de Biología; Facultad de Ciencias Naturales y Matemáticas; Universidad Distrital Francisco José de Caldas; Carrera 10 N° 19-62; Bogota; Colombia.
Department of Invertebrate Evolution; Institute of Zoology and Biomedical Research; Jagiellonian University; Gronostajowa 9; 30- 387 Kraków; Poland
Lepidoptera Andes colour patterns male genitalia molecular data

Abstract

Phylogenetic relationships of the predominantly Andean species-rich nymphalid genus Perisama are explored based on five genetic markers and a total of 3719 bps, and morphological characters of the adults with an emphasis on male genitalia and wing colour patterns. Its monophyly is recovered by including the genera Orophila, which turns out polyphyletic, and Mesotaenia. Two main, highly supported clades are identified, one comprising P. bomplandii and P. oppelii, the other all the remaining species. It is estimated that Perisama and its sister genus Diaethria diverged in Miocene, whereas its main radiation occurred in later Pliocene and throughout Pleistocene and into Holocene, simultaneously with the final Andean uplift. Alpha-taxonomic revision of Perisama was made. Based on comprehensive taxon sampling it is shown that colour patterns are less stable on a geographic scale than previously considered, thus several subspecies were synonymized. An updated checklist is presented. Male genitalia confirm as a more reliable taxonomic character for specific identification of Perisama.

 

References

  1. Attal, S. & De Marmels, J. (2012) Le genre Perisama Doubleday, 1849, présent à Auyan-Tepui (Venezuela) avec une nouvelle espèce (Lepidoptera, Nymphalidae). Bulletin de la Société entomologique de France, 117 (1), 111–113. https://doi.org/10.3406/bsef.2012.2648
  2. Attal, S. & Crosson du Cormier, A. (1996) The Genus Perisama: Lepidoptera Nymphalidae. Fédération Française des Sociétés de Sciences Naturelles, Paris, 149 pp.
  3. Attal, S. & Crosson du Cormier, A. (1997) Papillons néotropicaux nouveaux des genres Perisama et Epiphile (Lepidoptera Nymphalidae). Bulletin de la Société entomologique de France, 102 (3), 287–291. https://doi.org/10.3406/bsef.1997.17345
  4. Attal, S. & Crosson du Cormier, A. (2010) Le Genre Perisama Doubleday, 1849. Actualisation (Lepidoptera, Nymphalidae). Lambillionea, 110 (2), 227–236.
  5. Bonebreak, T.C, Ponisio, L.C, Boggs, C.L & Ehrlich, P.R. (2010) More than just indicators: A review of tropical butterfly ecology and conservation. Biological Conservation, 143 (8), 1831–1841. https://doi.org/10.1016/j.biocon.2010.04.044
  6. BEAST Developers. (2017) Effective Sample Size (ESS), BEAST Documentation. Available from: https://beast.community/ess_tutorial/ (accessed 6 September 2023)
  7. Bell, M.A. & Lloyd, G.T. (2015) Strap: an R package for plotting phylogenies against stratigraphy and assessing their stratigraphic congruence. Palaeontology, 58, 379–389. https://doi.org/10.1111/pala.12142
  8. Bouckaert, R.R. & Drummond, A.J. (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Ecology and Evolution, 17, 1–11. https://doi.org/10.1186/s12862-017-0890-6
  9. Bouckaert, R., Vaughan, T.G., Barido-Sottani J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F.K., Müller, N.F., Ogilvie, H.A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, C.-H., Xie, D., Zhang, C., Stadler, T. & Drummond, A.J. (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15, 1–28. https://doi.org/10.1371/journal.pcbi.1006650
  10. Brower, A.V.Z. (2000) Phylogenetic relationships among the Nymphalidae (Lepidoptera), inferred from partial sequences of the wingless gene. Proceedings of the Royal Society B, 267, 1201–1211. https://doi.org/10.1098/rspb.2000.1129
  11. Bryk, F. (1953) Lepidoptera aus dem Amazonasgebiete und aus Peru gesammelt von Dr. Douglas Melin und Dr. Abraham Roman. Arkiv för Zoologi, New Series, 5 (1), 1–268.
  12. Chazot, N., Wahlberg, N., Freitas A.V.L., Mitter, C., Labandeira, C., Sohn, J.C., Sahoo. R.K., Seraphim, N., de Jong, R. & Heikkilä, M. (2019). Priors and Posteriors in Bayesian Timing of Divergence Analyses: The Age of Butterflies Revisited. Systematic Biology, 68 (5), 797–813. https://doi.org/10.1093/sysbio/syz002
  13. Chazot, N., Condamine, F., Dudas, G., Peña, C., Kodandaramaiah, U., Matos-Maraví, P., Aduse-Poku, K., Elias, M., Warren, A.D., Lohman, D., Penz, C., DeVries, P., Fric, Z.F., Nylin, S., Müller, C., Kawahara, A.Y., Silva-Brandao, K., Lamas, G., Kleckova, I., Zubek, A., Ortiz-Acevedo, E., Vila, R., Vane-Wright, R., Mullen, S., Jiggins, C.D., Wheat, C.W., Freitas, A.V.L. & Wahlberg, N. (2021) Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies. Nature Communications, 12, 5717. https://doi.org/10.1038/s41467-021-25906-8
  14. Chernomor, O., von Haeseler & A., Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology, 65: 997–1008. https://doi.org/10.1093/sysbio/syw037
  15. Costa, M., Viloria, A.V.L., Huber, O., Attal, S. & Orellana, A. (2019) Lepidoptera del Pantepui. Parte I: Endemismo y caracterización biogeográfica. Entomotropica, 28 (3), 193–217.
  16. d’Abrera, B. (1987) Butterflies of the Neotropical Region. Part IV Nymphalidae. Hill House, Victoria, 152 pp.
  17. Descimon, H. & Mast, J. (1995) Nouvelles formes péruviennes du genre Perisama (Nymphalidae). Lambillionea, 95 (1), 9–18, pl. 1.
  18. Doubleday, E. (1847) The genera of diurnal Lepidoptera: comprising their generic characters, a notice of their habits and transformations, and a catalogue of the species of each genus. Longman, Brown, Green and Longmans, London, pp. 185–192. https://doi.org/10.5962/bhl.title.14057
  19. Felder, C. & Felder, R. (1861) Lepidoptera nova Columbiae. Wiener entomologische Monatschrift, 5 (3), 72–87.
  20. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
  21. Freitas A.V.L. & Brown K.Jr. (2004) Phylogeny of the Nymphalidae (Lepidoptera). Systematic Biology, 53 (3), 363–383. https://doi.org/10.1080/10635150490445670
  22. Freitas, A.V.L., Kaminski, L.A., Iserhard, C.A., Magaldi, L.M., Wahlberg, N., Silva-Branda, K.L. & Mielke, O.H.H. (2014) Paulogramma hydarnis (n. comb.) (Nymphalidae: Biblidinae): distribution, systematic position, and conservation status of a rare and endangered butterfly. Neotropical Entomology, 43, 218–226. https://doi.org/10.1007/s13744-014-0200-6
  23. Fruhstorfer, H. (1916) Neue neotropische Nymphaliden. Entomologische Zeitschrift, 29 (25), 97–98.
  24. Greeney, H.F., Dyer, L.A., DeVries, P.J., Walla, T.R., Salazar, V., Simbaña, W. & Salgaje, L. (2010) Early stages and natural history of Perisama oppelii (Latreille, 1811) (Nymphalidae, Lepidoptera) in eastern Ecuador. Kempffiana, 6, 16–30.
  25. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate Maximum-Likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. https://doi.org/10.1093/sysbio/syq010
  26. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
  27. Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518–522. https://doi.org/10.1093/molbev/msx281
  28. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haesele,r A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  29. Kirby, W.F. (1871) A synonymic catalogue of the diurnal Lepidoptera. John Van Voorst, London, vii + 690 pp. https://doi.org/10.5962/bhl.title.23779
  30. Lamas, G. (2004) Atlas of Neotropical Lepidoptera. Vol. 5A. Checklist: 4A. Hesperioidea-Papilionoidea. Association For Tropical Lepidoptera, Gainesville, Florida, pp. 245–247.
  31. Le Crom, J.-F. & Attal, S. (2013) Perisama oppelii (Latreille, 1809) dans la Sierra Nevada de Santa Marta en Colombie: une nouvelle sous-espèce (Lepidoptera, Nymphalidae). Lambillionea, CXIII (2), 1–5.
  32. Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
  33. Jenkins, D.W. (1983) Neotropical Nymphalidae. I. Revision of Hamadryas. Bulletin of the Allyn Museum, 81, 1–146.
  34. 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..LH., 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., Naïve, 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
  35. Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. https://doi.org/10.1007/BF01731581
  36. Klots, A.B. (1970) Lepidoptera. In: Tuxen, S.L. (Ed.), Taxonomist’s glossary of genitalia in insects. Munksgaard, Kopenhaga, pp. 115–130.
  37. Leite, L., Bonfantti, D., Lidke, A.L., Casagrande, M. & Mielke, O. (2017) Comparative study on the hypandrium of the Neotropical Biblidinae (Lepidoptera: Nymphalidae). SHILAP Revista de lepidopterologia, 45, 263–282. https://doi.org/10.57065/shilap.1001
  38. Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. https://doi.org/10.1038/35002501
  39. Oberthür, C. (1916) La réalité l’idée de genre est démontrée par les Catagrammides. Etudes de lépidoptérologie comparée, 11, 7–121, figs. A–G, pls. 340–363.
  40. Ogilvie, H.A., Bouckaert, R.R. & Drummond, A.J. (2017) StarBEAST2 brings faster species tree inference and accurate estimates of substitution rates. Molecular biology and evolution, 34 (8), 2101–2114. https://doi.org/10.1093/molbev/msx126
  41. Peña, C. & Malm, T. (2012) VoSeq: a Voucher and DNA Sequence Web Application. PlosOne, 7, e39071. https://doi.org/10.1371/journal.pone.0039071
  42. Purser, B. (2015) Butterflies of the Andes: Their Biodynamics and Diversification. Pemberley Natural History Books BC, Iver, 251 pp.
  43. Pyrcz, T.W., Lachowska-Cierlik, D., Willmott, K. R., Mrozek, A., Mahecha-Jiménez, O., Fåhraeus, C., Boyer, P., Martín, S. & Espeland, M. (2023) A new genus in the diverse Andean Pedaliodes complex uncovered using target enrichment (Lepidoptera, Nymphalidae). Systematic Entomology, 48 (1), 163–177. https://doi.org/10.1111/syen.12568
  44. Rambaut, A. & Drummond, A.J. (2014) FigTree. Version 1.4.3. Availabe from: http://tree.bio.ed.ac.uk/software/figtree (accessed 19 March 2025)
  45. Rambaut, A., Suchard, M., Xie, D. & Drummond, A.J. (2014) MCMC Trace Analysis Package. Version 1.6. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 12 January 2022)
  46. Razowski, J. (1996) Słownik morfologii owadów. PWN, Warszawa-Kraków, 431 pp.
  47. Romero, F. (1997) Weinmannia sp. (Cunionaceae) planta hospedera de Mesotaenia vaninka volara Hewitson 1868 y Mesotaenia vaninka gonalia Fruhstorfer 1916 (Lepidoptera: Nymphalidae) en Venezuela. Boletín de Entomología venezolana, New Series, 12 (2), 155–156.
  48. Röber, J.K.M. (1915) 42. Gattung: Calithea Bsd.–47. Gattung: Cyclogramma Dbl. w: Seitz, A. (wyd.), Die Gross–Schmetterlinge der Erde. Alfred Kernen, Stuttgart, 5, 499–500, pl. 103, Fig. a.
  49. Schwanwitsch, B.N. (1924) On the groundplan of the wing-pattern in nymphalids and certain other families of rhopalocerous Lepidopetra. Proceedings of the Zoological Society of London B, 34, 509–528. https://doi.org/10.1111/j.1096-3642.1924.tb01511.x
  50. Schaus, W. (1913) New species of Rhopalocera from Costa Rica. Proceedings of the zoological Society of London, 1913 (3), 339–367. https://doi.org/10.1111/j.1469-7998.1913.tb06133.x
  51. Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87, 651–701. https://doi.org/10.1093/aesa/87.6.651
  52. Talavera, G., Lukhtanov, V.A., Pierce, N.E & Vila, R. (2013) Establishing criteria for higher-level classification using molecular data: the systematics of Polyommatus blue butterflies (Lepidoptera, Lycaenidae). Cladistics, 29 (2013), 166–192. https://doi.org/10.1111/j.1096-0031.2012.00421.x
  53. Wahlberg, N. & Wheat, C.W. (2008) Genomic outposts serve thephylogenomic pioneers: designing novel nuclear markers forgenomic DNA extractions of Lepidoptera. Systematic Biology, 57, 231–242. https://doi.org/10.1080/10635150802033006
  54. 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, 227–251. https://doi.org/10.1111/j.1095-8312.2005.00531.x
  55. Wahlberg, N., Leneveu, J., Kodandaramaiah, U., Peña, C., Nylin, S., Freitas, A.V.L. & Brower, A.V.Z. (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proceedings of the Royal Society B, 276, 4295–4302. https://doi.org/10.1098/rspb.2009.1303
  56. 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.
  57. Zubek, A., Lorenc-Brudecka, J. & Pyrcz, T.W. (2015) Hypandrium as a key character in resolving species-level taxonomy on the example of Perisama oppelii (Latreille) (Lepidoptera: Nymphalidae, Biblidinae). Zootaxa, 3990 (1), 32–40. https://doi.org/10.11646/zootaxa.3990.1.2
  58. Zubek, A., Pyrcz, T.W., Lorenc-Brudecka, J., Boyer, P., Cerdeña, J., Mahecha-Jimenez, O. & Huertas, B. (2017) Systematic revision of the Andean butterfly genus Orophila Staudinger, 1886 (Lepidoptera: Nymphalidae: Biblidinae). Zootaxa, 4258 (5), 443–446. https://doi.org/10.11646/zootaxa.4258.5.3

How to Cite

Zubek, A., Wahlberg, N., Boyer, P., Lorenc-Brudecka, J., Mahecha-J., O. & Pyrcz, T. (2025) Integrative taxonomy, phylogeny and distribution patterns of the diverse Neotropical cloud forest butterfly genus Perisama Doubleday (Nymphalidae, Biblidinae, Callicorini). Zootaxa, 5636 (1), 1–34. https://doi.org/10.11646/zootaxa.5636.1.1