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Type: Article
Published: 2021-11-30
Page range: 201-237
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Solving the cryptic diversity of the genus Manerebia Staudinger in northern Peru: description of new species and considerations on the biogeographical role of the Huancabamba Deflection (Nymphalidae: Satyrinae: Pronophilina)

Nature Education Centre, Jagiellonian University, Gronostajowa 5, 30–387 Kraków, Poland. Instituto de Ciencias Naturales ICN/Laboratorio de Ecología del Paisaje y Modelación de Ecosistemas ECOLMOD, Universidad Nacional de Colombia. Carrera 30 No.45-03, Bogotá D.C., Colombia
Nature Education Centre, Jagiellonian University, Gronostajowa 5, 30–387 Kraków, Poland.
Florida Natural History Museum, University of Florida, Gainesville, USA.
Universidad Nacional de San Agustín de Arequipa, Museo de Historia Natural, Av. Alcides Carrión s/n, Escuela de Biología UNSA, Arequipa, Perú. 
Nature Education Centre, Jagiellonian University, Gronostajowa 5, 30–387 Kraków, Poland.
Lotissement l’Horizon, 13610, Le Puy Sainte Réparade, France.
Universidad Nacional de San Agustín de Arequipa, Museo de Historia Natural, Av. Alcides Carrión s/n, Escuela de Biología UNSA, Arequipa, Perú. 
Department of Invertebrate Evolution, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30–387 Kraków, Poland
Nature Education Centre, Jagiellonian University, Gronostajowa 5, 30–387 Kraków, Poland. Department of Invertebrate Evolution, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30–387 Kraków, Poland.
Lepidoptera Cryptic diversity molecular systematics morphology biogeographical barriers

Abstract

The Huancabamba Deflection in the Andes of northern Peru and southern Ecuador is a pivotal area for Neotropical biogeography, where exceptional biodiversity coincides with high rates of endemism. These characteristics are well illustrated within the montane butterfly genus Manerebia Staudinger (Nymphalidae, Satyrinae). Here, six new, apparently endemic species, and two new subspecies, are described from this region: M. inducta Pyrcz & Willmott n. sp., M. ronda Pyrcz & Boyer, n. sp., M. ronda amplia Pyrcz & Boyer, n. ssp., M. punku Pyrcz & Farfán n. sp., M. huamanii Cerdeña & Pyrcz n. sp., M. placida Pyrcz & Willmott n. sp., M. granatus Willmott, Radford & Pyrcz n. sp. and M. prattorum udima Pyrcz & Boyer, n. ssp. A total of 22 species of Manerebia is reported from the study region, as much as half the total number of species in this genus distributed throughout the tropical Andes. The alpha-taxonomy of Manerebia is particularly demanding, as colour patterns have apparently converged among different species making identification virtually impossible in some cases without comparison of their genitalia, which prove taxonomically and phylogenetically highly valuable. On the other hand, several species differ markedly in wing colour patterns and occur at different elevations but have identical genitalia. Furthermore, our data show that DNA barcoding is only partly viable as an alpha-taxonomic tool, as some markedly different species of Manerebia, in terms of external morphology and ecological preferences, are genetically not separable using only COI markers. On the other hand, several species barely differing morphologically are identified based on barcode. Barcodes of 26 species, including 18 from the northern Andes, are studied here, showing strong differences within some taxa previously considered conspecific based on morphological characters, suggesting that their taxonomic status needs to be re-evaluated. In particular, M. trimaculata and the widely distributed polytypic M. inderena may be highly variable species or complexes of several species. A total of 16 species are found north of the Chamaya valley in southern Ecuador and extreme northern Peru, compared to 14 species south of it in northern Peru. The faunal (Jaccard) similarity coefficient of the two adjacent regions is low (0.3), reflecting the role of the Huancabamba Deflection as a biogeographical barrier.

 

References

  1. Albert, J.S. & Reis, R.E. (2011) Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley, California, 424 pp.
    Antonelli, A., Nylander, J.A., Persson, C. & Sanmartín, I. (2009) Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the National Academy of Sciences, 106 (24), 9749–29754.
    BEAST Developers (2017) Effective Sample Size (ESS), BEAST Documentation. Available from: https://beast.community/ess_tutorial/(accessed 7 January 2021)
    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, F., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, C.H., Xie, D., Zhang, C., Stadle, T. & Drummond, A.J. (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15 (4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650
    Cadena, C.D. & Zapata, F. (2021) The genomic revolution and species delimitation in birds (and other organisms): Why phenotypes should not be overlooked. The Auk: Ornithology, 138 (2), 1–18. https://doi.org/10.1093/ornithology/ukaa069
    Dobzhansky, T. (1935) A critique of the species concept in biology. Philosophy of Science, 2 (3), 344–355.
    Drummond, A.J., Ashton, B., Buxton, S., Cheung M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A. (2009) Geneious v. 4.8.5. Available from: http://www.geneious.com/(accessed 3 April 2021)
    Duellman, W.E. (1979) The herpetofauna of the Andes: patterns of distribution, origin, differentiation, and present communities. University of Kansas Museum of Natural History Monograph, 7, 371–459.
    Duellman, W.E. & Pramuk, J.B. (1999) Frogs of the genus Eleutherodactylus (Anura: Leptodactylidae) in the Andes of northern Peru. Scientific Papers Natural History Museum The University of Kansas, 13, 1–78.
    Escalona, M., La Marca, E., Castellanos, M., Fouquet, A., Crawford, A.J., Rojas-Runjaic, F.J.M., Giaretta, A.A., Señaris, J.C. & Castroviejo-Fisher, S. (2021) Integrative taxonomy reveals a new but common Neotropical treefrog, hidden under the name Boana xerophylla. Zootaxa, 4981 (1), 401–448. https://doi.org/10.11646/zootaxa.4981.3.1
    Free Software Foundation, Inc. (1991) Inkscape 0.92.3 (2405546), Boston, MA 02110-1301, USA. Available from: https://www.inkscape.org/(accessed 6 June 2021)
    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.
    García-Melo, J.E., Oliveira, C., Da Costa Silva, G.J., Ochoa-Orrego, L.E., Garcia-Pereira, L.H. & Maldonado-Ocampo, J.A. (2019) Species delimitation of neotropical Characins (Stevardiinae): Implications for taxonomy of complex groups. PLoS ONE, 14 (6), e0216786. https://doi.org/10.1371/journal.pone.0216786
    Gernhard, T. (2008) The conditioned reconstructed process. Journal of Theoretical Biology, 253 (4), 769–778. https://doi.org/10.1016/j.jtbi.2008.04.005
    Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2017) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518–522.
    Kalyaanamoorthy, S., Minh, B., Wong, T., Von Haeseler, 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
    Katoh, K. & Standley, D.M. (2014) MAFFT: iterative refinement and additional methods. Methods in Molecular Biology, 1079, 131–146.
    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.
    Klots, A.B. (1956) Lepidoptera. In: Tuxen, S.L. (Eds.), Taxonomist’s glossary of genitalia in insects. Ejnar Munksgaard, Copenhagen, pp. 97–110.
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35,1547–1549.
    Lamas, G. (1982) A preliminary zoogeographical division of Peru, based on butterfly distributions (Lepidoptera, Papilionoidea). In: Prance, T. (Eds.), The Biological Model for Diversification in the Tropics. Columbia University Press, New York, pp. 336–357.
    Lamas, G., Viloria, A.L. & Pyrcz, T.W. (2004) Tribe Satyrini, Subtribe Pronophilina. In: Lamas, G. (Eds.), Checklist. Part 4A. Hesperioidea—Papilionoidea. Association for Tropical Lepidoptera Scientific Publishers, Gainesville, Florida, pp. 206–215.
    Linares-Palomino, R. (2006) Phytogeography and floristics of seasonally dry tropical forests in Peru. In: Pennington, R.T., Lewis, G.P. & Ratter, J.A. (Eds.), Neotropical Savannas and Seasonally Dry Forests: Plant Diversity, Biogeography, and Conservation. Vol. 69. The Systematics Association Special Volume. Taylor and Francis Group, London, pp. 257–280. https://doi.org/10.1201/9781420004496.ch11
    Mahecha, O., Garlacz, R., Andrade, M.G., Prieto, C. & Pyrcz, T.W. (2019) Island biogeography in continental areas: inferring dispersal based on distributional patterns of Pronophilina butterflies (Nymphalidae: Satyrinae) in the north Andean massifs. Revista Mexicana de Biodiversidad, 90, e902796. https://doi.org/10.22201/ib.20078706e.2019.90.2796
    Mahecha-J., O., Triviño, P., Andrade-C, M.G. & Pyrcz, T.W. (2021) Two new species of Manerebia Staudinger from paramo habitat in the Colombian Eastern Cordillera of the Andes (Lepidoptera: Nymphalidae, Satyrinae, Pronophilina). Zootaxa, 4970 (2), 293–302. https://doi.org/10.11646/zootaxa.4970.2.3
    Marín, M.A., Cadavid, I.C., Valdés, L., Álvarez, C.F., Uribe, S.I., Vila, R. & Pyrcz, T.W. (2017) DNA Barcoding of an Assembly of Montane Andean Butterflies (Satyrinae): Geographical Scale and Identification Performance. Neotropical Entomology, 46, 514–523.
    Matos-Maraví, P., Wahlberg, N., Antonelli, A. & Penz, C.M. (2019) Species limits in butterflies (Lepidoptera: Nymphalidae): Reconciling classical taxonomy with the multispecies coalescent. Systematic Entomology, 44 (4), 745–756.
    Maurin, K. (2020). A dated phylogeny of the genus Pennantia (Pennantiaceae) based on whole chloroplast genome and nuclear ribosomal 18S–26S repeat region sequences. PhytoKeys, 155, 15–32. https://doi.org/10.3897/phytokeys.155.53460
    Mayr, E. (1957) Species concepts and definitions. In: Mayr, E. (Eds.), The Species Problem. American Association for the Advancement of Science, Washington, D.C., pp. 1–22.
    Minh, B.Q., Nguyen, M.A.T. & Von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30 (5), 1188–1195.
    Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A. & Lanfear, R. (2020) IQ–TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37 (5), 1530–1534.
    Mitouard, P., Kissel, C. & Laj, C. (1990) Post–Oligocene rotations in southern Ecuador and northern Peru and the formation of the Huancabamba deflection in the Andean Cordillera. Earth and Planetary Science Letters, 98, 329–339.
    National Center for Biotechnology Information [NCBI] (1988) National Library of Medicine (US), Bethesda, Maryland. Available from: https://www.ncbi.nlm.nih.gov/nuccore/(accessed 12 October 2020)
    Núñez, R., Genaro, J.A., Pérez-Asso, A., Murillo-Ramos, L., Janzen, D.H., Hallwachs, W., Wahlberg, N. & Hausmann, A. (2020) Species delimitation and evolutionary relationships among Phoebis New World sulphur butterflies (Lepidoptera, Pieridae, Coliadinae). Systematic Entomology, 45 (2), 481–492.
    Opgenoorth, L., Hofmann, S. & Schmidt, J. (2020) Rewinding the molecular clock in the genus Carabus (Coleoptera: Carabidae): Revisiting Andujar et al. in light of new fossil evidence and the Gondwana split. bioRxiv, 2020.02.19.912543. https://doi.org/10.1101/2020.02.19.912543
    Pan, T., Sun, Z., Lai, X., Orozcoterwengel, P., Yan, P., Wu, G., Wanga, H., Zhuc,W., Wu, X. & Zhang, B. (2019) Hidden species diversity in Pachyhynobius: A multiple approaches species delimitation with mitogenomes. Molecular Phylogenetics and Evolution, 137, 138–145.
    Peña, C., Wahlberg, N., Weingartner, E., Kodandaramaiah, U., Nylin, S., Freitas, A.V. & Brower, A.V.Z. (2006) Higher level phylogeny of Satyrinae butterflies (Lepidoptera: Nymphalidae) based on DNA sequence data. Molecular Phylogenetics and Evolution, 40 (1), 29–49.
    Peña, C., Nylin, S. & Wahlberg, N. (2011) The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods. Zoological Journal of the Linnean Society, 161 (1), 64 –87.
    Pola, L., Hejduk, V., Zíka, A., Winkelhöfer, T., Šmíd, J., Carranza, S., Shobrak, M., Baker, M. & Amr, Z.S. (2021) Small and overlooked: Phylogeny of the genus Trigonodactylus (Squamata: Gekkonidae), with the first record of Trigonodactylus arabicus from Jordan. Saudi Journal of Biological Sciences, 28 (6), 3511–3516.
    Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin W.D. & Vogler, A. (2006) Sequence–Based Species Delimitation for the DNA Taxonomy of Undescribed Insects. Systematic Biology, 55, 595–609. [PMID: 16967577] https://doi.org/10.1080/10635150600852011.
    Pyrcz, T.W. (1999) The E. Krüger collection of pronophiline butterflies, Part 2: genera Manerebia to Thiemeia. Lambillionea, 99, 351–376.
    Pyrcz, T.W. (2004) Pronophiline butterflies of the highlands of Chachapoyas in northern Peru: faunal survey, diversity and distribution patterns (Lepidoptera, Nymphalidae, Satyrinae). Genus, 15, 455–622.
    Pyrcz, T.W., Willmott, K.R., Hall, J.P.W. & Viloria, A.L. (2006) A review of the genus Manerebia Staudinger (Lepidoptera: Nymphalidae: Satyrinae) in the northern Andes. Journal of Research on the Lepidoptera, 39, 37–79.
    Pyrcz, T.W. (2010) Wybrane zagadnienia z taksonomii, zoogeografii i ewolucji faun górskich na przykładzie grupy modelowej motyli z plemienia Pronophilini (Nymphalidae). Mantis, Olsztyn, 245 pp.
    Pyrcz, T.W., Cerdeña, J. & Villalobos, H. (2013) Systematics, bionomics and zoogeography of high Andean pedaliodines. Part 14: Two new species of Pedaliodes Butler from the Huancabamba Deflection in southern Ecuador and northern Peru (Lepidoptera: Nymphalidae: Satyrinae). Genus, 24, 131–141.
    Quintana, C., Pennington, R.T., Ulloa, C.U. & Balslev, H. (2017) Biogeographic Barriers in the Andes: Is the Amotape—Huancabamba Zone a Dispersal Barrier for Dry Forest Plants? Annals of the Missouri Botanical Garden, 102 (3), 542–550.
    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 15 May 2021)
    Ramos, V.A. (2009) Anatomy and global context of the Andes: Main geologic features and the Andean orogenic cycle. In: Kay, S.M., Ramos, V.A. & Dickinson, W.R. (Eds.), Backbone of the Americas: Shallow Subduction, Plateau Uplift, and Ridge and Terrane Collision. Geological Society of America Memoir, GSA, Boulder, pp. 31–65.
    Ratnasingham, S. & Hebert, P.D. (2007) BOLD: The Barcode of Life Data System (http://www. barcodinglife.org). Molecular Ecology Notes, 7, 355–364.
    Razowski, J. (1996) Słownik morfologii owadów. PWN, Warszawa-Kraków, 431 pp.
    Rubinoff, D., San Jose, M. & Hundsdoerfer, A.K. (2021) Cryptic diversity in a vagile Hawaiian moth group suggests complex factors drive diversification. Molecular Phylogenetics and Evolution, 155, 107002. https://doi.org/10.1016/j.ympev.2020.107002
    Shen, Y., Hubert, N., Huang, Y., Wang, X., Gan, X., Peng, Z. & He, S. (2019) DNA barcoding the ichthyofauna of the Yangtze River: Insights from the molecular inventory of a mega- iverse temperate fauna. Molecular Ecology Resources, 19 (5), 1278–1291.
    Steinmann, M., Hungerbuhler, D., Seward, D. & Winkler, W. (1999) Neogene tectonic evolution and exhumation of the southern Ecuadorian Andes: A combined stratigraphy and fission–track approach. Tectonophysics, 307, 255–276.
    Torres-Carvajal, O., Venegas, P.J. & Nunes, P.M.S. (2020) Description and Phylogeny of a New Species of Andean Lizard (Gymnophthalmidae: Cercosaurinae) from the Huancabamba Depression. South American Journal of Herpetology, 18 (1), 13–23.
    Viloria, A.L. (2007) Some Gondwanan and Laurasian elements in the satyrine fauna of South America (Lepidoptera: Nymphalidae: Satyrinae). Tropical Lepidoptera, 15, 53–55.
    Wahlberg, N. & Wheat, C.W. (2008) Genomic Outposts Serve the Phylogenomic Pioneers: Designing Novel Nuclear Markers for Genomic DNA Extractions of Lepidoptera. Systematic Biology, 57 (2), 231–242.
    Weigend, M. (2002) Observations on the Biogeography of the Amotape–Huancabamba Zone in Northern Peru. The Botanical Review, 68, 38–54.
    Willmott, K.R., Lamas, G., Radford, J., Marín, M.A., Nakahara, S., Espeland, M., Xiao, L. & Hall, J.P.W. (2018) A distinctive new species of cloud forest Euptychiina (Lepidoptera: Nymphalidae: Satyrinae) from Ecuador and Peru. Tropical Lepidoptera Research, 28, 39–45.
    Young, K.R. & Reynel, C. (1997) Huancabamba Region, Peru and Ecuador. In: Davis, S.D., Heywood, V.H., Herrera-MacBryde, O., Villa-Lobos, J. & Hamilton, A.C. (Eds.), Centers of Plant Diversity, a Guide and Strategy for their Conservation. Vol. 3. The Americas IUCN Publications Unit, Cambridge, pp. 465–469.
    Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.
    Zubek, A., Pyrcz, T.W. & Boyer, P. (2014) Description of a New Species of the Andean Butterfly Genus Forsterinaria Gray (Lepidoptera: Nymphalidae) with Considerations on an Apparently New Structure in Male Genitalia. Neotropical Entomology, 43, 68–77.

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