Assessing a generic synapomorphy of Pseudodebis Forster, 1964 (Lepidoptera : Nymphalidae : Satyrinae) and a recent speciation with a shift in elevation between two new species in the western Andes
Shinichi Nakahara A B C F , Pável Matos-Maraví D , Johanna Schwartz E and Keith R. Willmott AA McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.
B Department of Entomology, University of Florida, Gainesville, FL 32611, USA.
C Departamento de Entomología, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru.
D Biology Centre of the Czech Academy of Sciences, Institute of Entomology, CZ-370 05 České Budějovice, Czech Republic.
E Department of Entomology, The Ohio State University, Columbus, OH 43210, USA.
F Corresponding author. Email: snakahara@ufl.edu
Invertebrate Systematics 35(2) 158-180 https://doi.org/10.1071/IS20024
Submitted: 7 April 2020 Accepted: 19 August 2020 Published: 8 February 2021
Abstract
The field of systematics and our understanding of phylogenetic relationships have been invigorated by the use of molecular data, but analyses based on DNA sequence data are not always corroborated by diagnostic morphological characters. In particular, several taxonomic changes in butterflies (Papilionoidea) have been made solely on the basis of molecular data without identifying morphological synapomorphies that might have aided in diagnosing taxa from butterfly collections or specimens with no accessible DNA. We here focus on the butterfly genus Pseudodebis Forster, 1964 in the so-called ‘Taygetis clade’, which is one of the major clades in the diverse Neotropical nymphalid subtribe Euptychiina. We inferred the evolution of a male genitalic character using the most comprehensive molecular phylogeny for the ‘Taygetis clade’ to date. This approach allowed us to identify a synapomorphy for Pseudodebis Forster, 1964, which can be used to morphologically diagnose this genus and to distinguish it from other genera in the ‘Taygetis clade’. In addition, we describe two new species of Pseudodebis, P. nakamurai Nakahara & Willmott, sp. nov. and P. pieti Nakahara & Willmott, sp. nov., recovered as sister species based on molecular data, with an estimated time of divergence of 0.3 Ma (Bayesian confidence interval 0.03–1.61 Ma). Despite the low genetic divergence between these two Pseudodebis species, they can be readily distinguished by wing morphology. Pseudodebis nakamurai, sp. nov. and P. pieti, sp. nov. occur in partial sympatry across an elevational gradient along the western Andes, and the inferred recent speciation event might be related to a shift in elevation and possibly a change in larval hostplant preference.
urn:lsid:zoobank.org:pub:38B4AF76-79E9-4D4D-BF16-FCD8F53A7277
Keywords: ancestral state reconstruction, Neotropics, SIMMAP, synapomorphy, tropical Andes.
References
Anisimova, M., Gil, M., Dufayard, J. F., Dessimoz, C., and Gascuel, O. (2011). Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Systematic Biology 60, 685–699.| Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes.Crossref | GoogleScholarGoogle Scholar | 21540409PubMed |
Augustyn, W. J., Anderson, B., van der Merwe, J. F., and Ellis, A. G. (2017). Spatial turnover in host-plant availability drives host-associated divergence in a South African leafhopper (Cephalelus uncinatus). BMC Evolutionary Biology 17, 72.
| Spatial turnover in host-plant availability drives host-associated divergence in a South African leafhopper (Cephalelus uncinatus).Crossref | GoogleScholarGoogle Scholar | 28274200PubMed |
Bereczki, J., Póliska, S., Váradi, A., and Tóth, J. P. (2020). Incipient sympatric speciation via host race formation in Phengaris arion (Lepidoptera: Lycaenidae). Organisms, Diversity & Evolution 20, 63–76.
| Incipient sympatric speciation via host race formation in Phengaris arion (Lepidoptera: Lycaenidae).Crossref | GoogleScholarGoogle Scholar |
Bollback, J. P. (2006). SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7, 88.
| SIMMAP: stochastic character mapping of discrete traits on phylogenies.Crossref | GoogleScholarGoogle Scholar | 16504105PubMed |
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M. A., Rambaut, A., and Drummond, A. J. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| BEAST 2: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar | 24722319PubMed |
Bremer, B., Jansen, R. K., Oxelman, B., Backland, M., Lantz, H., and Kim, K. J. (1999). More characters or more taxa for a robust phylogeny – case study from the coffee family (Rubiaceae). Systematic Biology 48, 413–435.
| More characters or more taxa for a robust phylogeny – case study from the coffee family (Rubiaceae).Crossref | GoogleScholarGoogle Scholar | 12066290PubMed |
Brues, C. T. (1924). The specificity of food plants in the evolution of phytophagous insects. American Naturalist 58, 127–144.
| The specificity of food plants in the evolution of phytophagous insects.Crossref | GoogleScholarGoogle Scholar |
Bush, G. L. (1969). Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera: Tephritidae). Evolution 23, 237–251.
| Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera: Tephritidae).Crossref | GoogleScholarGoogle Scholar | 28562891PubMed |
Chazot, N., Wahlberg, N., Freitas, A. V. L., Mitter, C., Labandeira, C., Sohn, J. C., Sahoo, R. K., Seraphim, N., de Jong, R., and Heikkilä, M. (2019). Priors and posteriors in Bayesian timing of divergence analyses: the age of butterflies revisited. Systematic Biology 68, 797–813.
| Priors and posteriors in Bayesian timing of divergence analyses: the age of butterflies revisited.Crossref | GoogleScholarGoogle Scholar | 30690622PubMed |
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |
Elias, M., Hill, R., Dasmahapatra, K., Willmott, K. R., Brower, A., Mallet, J., and Jiggins, C. (2007). Limited performance of DNA barcoding in a diverse community of tropical butterflies. Proceedings. Biological Sciences 274, 2881–2889.
| Limited performance of DNA barcoding in a diverse community of tropical butterflies.Crossref | GoogleScholarGoogle Scholar | 17785265PubMed |
Espeland, M., Breinholt, J. W., Barbosa, E. P., Casagrande, M. M., Huertas, B., Lamas, G., Marín, M. A., Mielke, O. H. H., Miller, J. Y., Nakahara, S., Tan, D., Warren, A. D., Zacca, T., Kawahara, A. Y., Freitas, A. V. L., and Willmott, K. R. (2019). Four hundred shades of brown: higher level phylogeny of the problematic Euptychiina (Lepidoptera, Nymphalidae, Satyrinae) based on hybrid enrichment data. Molecular Phylogenetics and Evolution 131, 116–124.
| Four hundred shades of brown: higher level phylogeny of the problematic Euptychiina (Lepidoptera, Nymphalidae, Satyrinae) based on hybrid enrichment data.Crossref | GoogleScholarGoogle Scholar | 30423438PubMed |
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar | 28561359PubMed |
Ferreira, V. S., Keller, O., Branham, M. A., and Ivie, M. A. (2019). Molecular data support the placement of the enigmatic Cheguevaria as a subfamily of Lampyridae (Insecta: Coleoptera). Zoological Journal of the Linnean Society 187, 1253–1258.
| Molecular data support the placement of the enigmatic Cheguevaria as a subfamily of Lampyridae (Insecta: Coleoptera).Crossref | GoogleScholarGoogle Scholar |
Forster, W. (1964). Beiträge zur kenntnis der insektenfauna Boliviens XIX. Lepidoptera III. Satyridae. Veröffentlichungen der Zoologischen Staatssammlung München 8, 51–88.
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 20525638PubMed |
Haldane, J. B. S. (1959). Natural selection. In ‘Darwin’s Biological Work’. (Ed. P. R. Bell.) pp. 101–149. (Cambridge University Press.)
Hausmann, A., Haszprunar, G., Segerer, A. H., Speidel, W., Behounek, G., and Hebert, P. D. N. (2011). Now DNA-barcoded: the butterflies and larger moths of Germany. Spixiana 34, 47–58.
Hebert, P. D. N., deWaard, J. R., and Landry, J. F. (2010). DNA barcodes for 1/1000 of the animal kingdom. Biology Letters 6, 359–362.
| DNA barcodes for 1/1000 of the animal kingdom.Crossref | GoogleScholarGoogle Scholar |
Hill, R. I., Elias, M., Dasmahapatra, K. K., Jiggins, C. D., Koong, V., Willmott, K. R., and Mallet, J. (2012). Ecologically relevant cryptic species in the highly polymorphic Amazonian butterfly Mechanitis mazaeus sensu lato (Lepidoptera: Nymphalidae; Ithomiini). Biological Journal of the Linnean Society. Linnean Society of London 106, 540–560.
| Ecologically relevant cryptic species in the highly polymorphic Amazonian butterfly Mechanitis mazaeus sensu lato (Lepidoptera: Nymphalidae; Ithomiini).Crossref | GoogleScholarGoogle Scholar |
Hillis, D. M. (1987). Molecular versus morphological approaches to systematics. Annual Review of Ecology and Systematics 18, 23–42.
| Molecular versus morphological approaches to systematics.Crossref | GoogleScholarGoogle Scholar |
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q., and Vinh, L. S. (2018). UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518–522.
| UFBoot2: improving the ultrafast bootstrap approximation.Crossref | GoogleScholarGoogle Scholar | 29077904PubMed |
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., and Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589.
| ModelFinder: fast model selection for accurate phylogenetic estimates.Crossref | GoogleScholarGoogle Scholar | 28481363PubMed |
Lamas, G. (2004). Nymphalidae. Satyrinae. Tribe Satyrini. Subtribe Euptychiina. Checklist: Part 4A. Hesperioidea – Papilionoidea. In ‘Atlas of Neotropical Lepidoptera. Volume 5A’. (Ed. J. B. Heppner.) pp. 217–223. (Association for Tropical Lepidoptera; Scientific Publishers; Gainesville, FL, USA.)
Lancaster, L. T. (2020). Host use diversification during range shifts shapes global variation in Lepidopteran dietary breadth. Nature Ecology & Evolution 4, 963–969.
| Host use diversification during range shifts shapes global variation in Lepidopteran dietary breadth.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2017). Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| 28013191PubMed |
Marín, M. A., Peña, C., Uribe, S. I., and Freitas, A. V. L. (2017). Morphology agrees with molecular data: phylogenetic affinities of Euptychiina butterflies (Nymphalidae: Satyrinae). Systematic Entomology 42, 768–785.
| Morphology agrees with molecular data: phylogenetic affinities of Euptychiina butterflies (Nymphalidae: Satyrinae).Crossref | GoogleScholarGoogle Scholar |
Matos-Maraví, P. F., Peña, C., Willmott, K. R., Freitas, A. V., and Wahlberg, N. (2013). Systematics and evolutionary history of butterflies in the ‘Taygetis clade’ (Nymphalidae: Satyrinae: Euptychiina): towards a better understanding of Neotropical biogeography. Molecular Phylogenetics and Evolution 66, 54–68.
| Systematics and evolutionary history of butterflies in the ‘Taygetis clade’ (Nymphalidae: Satyrinae: Euptychiina): towards a better understanding of Neotropical biogeography.Crossref | GoogleScholarGoogle Scholar | 23000820PubMed |
Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., and Lanfear, R. (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.
| IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era.Crossref | GoogleScholarGoogle Scholar | 32011700PubMed |
Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., Frandsen, P. B., Ware, J., Flouri, T., Beutel, R. G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A. J., et al. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767.
| Phylogenomics resolves the timing and pattern of insect evolution.Crossref | GoogleScholarGoogle Scholar | 25378627PubMed |
Murray, D., and Prowell, D. P. (2005). Molecular phylogenetics and evolutionary history of the neotropical satyrine Subtribe Euptychiina (Nymphalidae: Satyrinae). Molecular Phylogenetics and Evolution 34, 67–80.
| Molecular phylogenetics and evolutionary history of the neotropical satyrine Subtribe Euptychiina (Nymphalidae: Satyrinae).Crossref | GoogleScholarGoogle Scholar | 15579382PubMed |
Nakahara, S., Vega, G., and Willmott, K. R. (2016). Description of a new species of Euptychia Hübner, 1818 (Lepidoptera: Nymphalidae: Satyrinae) from the western Andes. Zootaxa 4184, 358–366.
| Description of a new species of Euptychia Hübner, 1818 (Lepidoptera: Nymphalidae: Satyrinae) from the western Andes.Crossref | GoogleScholarGoogle Scholar | 27811644PubMed |
Nakahara, S., Willmott, K. R., Mielke, O. H. H., Schwartz, J., Zacca, T., Espeland, M., and Lamas, G. (2018a). Seven new taxa from the butterfly subtribe Euptychiina (Lepidoptera: Nymphalidae: Satyrinae) with revisional notes on Harjesia Forster, 1964 and Pseudeuptychia Forster, 1964. Insecta Mundi 0639, 1–38.
Nakahara, S., Zacca, T., Huertas, B., Neild, A. F. E., Hall, J. P. W., Lamas, G., Holian, L. A., Espeland, M., and Willmott, K. R. (2018b). Remarkable sexual dimorphism, rarity and cryptic species: a revision of the ‘aegrota species group’ of the Neotropical butterfly genus Caeruleuptychia Forster, 1964 with the description of three new species (Lepidoptera, Nymphalidae, Satyrinae). Insect Systematics & Evolution 49, 130–182.
| Remarkable sexual dimorphism, rarity and cryptic species: a revision of the ‘aegrota species group’ of the Neotropical butterfly genus Caeruleuptychia Forster, 1964 with the description of three new species (Lepidoptera, Nymphalidae, Satyrinae).Crossref | GoogleScholarGoogle Scholar |
Nakahara, S., Matos-Maraví, P., Barbosa, E. P., Willmott, K. R., Lamas, G., and Freitas, A. V. L. (2019a). Two new species of Taygetina with a possible case of ‘juxta loss’ in butterflies (Lepidoptera: Nymphalidae: Satyrinae). Insect Systematics and Diversity 3, 9.
| Two new species of Taygetina with a possible case of ‘juxta loss’ in butterflies (Lepidoptera: Nymphalidae: Satyrinae).Crossref | GoogleScholarGoogle Scholar |
Nakahara, S., Zacca, T., Dias, F. M. S., Dolibaina, D. R., Xiao, L., Espeland, M., Casagrande, M. M., Mileke, O. H. H., Lamas, G., Huertas, B., Kleckner, K., and Willmott, K. R. (2019b). Revision of the poorly known Neotropical butterfly genus Zischkaia Forster, 1964 (Lepidoptera: Nymphalidae: Satyrinae), with description of nine new species. European Journal of Taxonomy 551, 1–67.
| Revision of the poorly known Neotropical butterfly genus Zischkaia Forster, 1964 (Lepidoptera: Nymphalidae: Satyrinae), with description of nine new species.Crossref | GoogleScholarGoogle Scholar |
Peña, C., Nylin, S., Freitas, A. V. L., and Wahlberg, N. (2010). Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae). Zoologica Scripta 39, 243–258.
| Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae).Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., and Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
| Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |
Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.
| phytools: an R package for phylogenetic comparative biology (and other things).Crossref | GoogleScholarGoogle Scholar |
Rosser, N., Freitas, A. V. L., Huertas, B., Joron, M., Lamas, G., Mérot, C., Simpson, F., Willmott, K. R., Mallet, J., and Dasmahapatra, K. A. (2019). Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies. Zoological Journal of the Linnean Society 186, 233–249.
| Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies.Crossref | GoogleScholarGoogle Scholar |
Stehr, F. W. (1987). ‘Immature Insects.’ (Kendall/Hunt Publishing: Dubuque, IA, USA.)
Sun, X., Bedos, A., and Deharveng, L. (2018). Unusually low genetic divergence at COI barcode locus between two species of intertidal Thalassaphorura (Collembola: Onychiuridae) PeerJ 6, e5021.
| Unusually low genetic divergence at COI barcode locus between two species of intertidal Thalassaphorura (Collembola: Onychiuridae)Crossref | GoogleScholarGoogle Scholar | 30083437PubMed |
Zhang, J., Cong, Q., Shen, J., Opler, P. A., and Grishin, N. V. (2019). Changes to North American butterfly names. The Taxonomic Report 8, 1–12.