Abstract
Andesiops peruvianus (Ulmer, 1920) is a small minnow mayfly with a distribution throughout the Andes Mountains, mainly in lotic environments. In recent years, the taxonomic status of the species has been shifting, even finding out molecular and morphological evidence to consider it as a cryptic species. In this work, we collected seven specimens of A. peruvianus from the Lake Titicaca in Peru, the type locality and perform molecular and morphological analyses to test their relationship with specimens from other regions. The species delimitation analysis revealed the existence of five MOTUs for specimens identified as A. peruvianus along the Andes Mountains, while the Lake Titicaca specimens formed a single MOTU with high interspecific distance. In this MOTU were found specimens with different types of abdominal gills, from translucent to markedly tracheated supporting the hypothesis of phenotypic plasticity at the abdominal gill level. Also, an extension in the range of tarsal claw denticles, from 10–12 to 10–14, were observed, higher than what were found in other regions. Our results support A. peruvianus as a species complex and reveal A. peruvianus from Titicaca as a single MOTU. Future morphological revisions of topotype specimens as well as from other Andean regions are required to strengthen the diagnosis of informative characteristics at both the larval and adult stage to elucidate the real status of the species.
References
Albrecht, C., Kroll, O., Moreno, E. & Wilke, T. (2009) Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biological Invasions, 11 (8), 1821–1826. https://doi.org/10.1007/s10530-008-9360-9
Baird, D. & Sweeney, B. (2011) Applying DNA barcoding in benthology: The state of the science. Journal of the North American Benthological Society, 30 (1), 122–124. https://doi.org/10.1899/10-154.1
Beltrán, L., Miserendino, M.L. & Pessacq, P. (2011) Life history, seasonal variation and pro-duction of Andesiops torrens (Lugo-Ortiz and McCafferty) and Andesiops peruvianus (Ulmer) (Ephemeroptera: Baetidae) in a headwater Patagonian stream. Limnologica, 41, 57–62. https://doi.org/10.1016/j.limno.2010.07.002
Berner, L. (1980) Ephemeroptera Nymphs. Proceedings of the Academy of Natural Sciences of Philadelphia, 132, 176–217.
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.H., Xie, D., Suchard, M.A., Rambaut, A. & Drummond, A.J. (2014) BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLOS Computational Biology, 10 (4), e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Caspers, H. (1979) The Ecology of Running Waters. Internationale Revue Der Gesamten Hydrobiologie Und Hydrographie, 64 (1), 1–70. https://doi.org/10.1002/iroh.19790640105
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9 (8), 1–2. https://doi.org/10.1038/nmeth.2109
Dejoux, C. (1991) Los Insectos. In: Dejoux, C. & Iltis, A. (Eds.), El lago Titicaca: Síntesis del conocimiento limnológico actual. ORSTOM & HISBOL, La Paz, pp. 371–386.
De León, L.F., Cornejo, A., Gavilán, R.G. & Aguilar, C. (2020) Hidden biodiversity in Neotropical streams: DNA barcoding uncovers high endemicity of freshwater macroinvertebrates at small spatial scales. PLoS ONE, 15 (8), e0231683. https://doi.org/10.1371/journal.pone.0231683
Demoulin, G. (1966) Contribution a L’Etude del Ephemeropteres du Surinam. Bulletin de l’Institute Royale des Sciences Naturales de Belgique, 42 (37), 1–22.
Desjardins, P. & Conklin, D. (2010) NanoDrop microvolime quantitation of nucleic acids. Journal of Visualized Experiements, 45, e2565.
Domínguez, E., Molineri, C. & Nieto, C. (2009) Ephemeroptera. In: Domínguez, D. & Fernández, R. (Eds.), Macroinvertebrados Bentónicos Sudamericanos. Fundación Miguel Lillo, Tucumán, pp. 55–93.
Eaton, A.E. (1881) An announcement of new genera of the Ephemeridae, Entomologist’s Monthly Magazine, 17, 191–197.
Ekrem, T., Stur, E. & Hebert, P. (2010) Females do count: Documenting Chironomidae (Diptera) species diversity using DNA barcoding. Organisms Diversity & Evolution, 10, 397–408. https://doi.org/10.1007/s13127-010-0034-y
Figueroa, R., Valdovinos, C., Araya, E. & Parra, O. (2003) Benthic macroinvertebrates as indicators of water quality of southern Chile rivers. Revista Chilena de Historia Natural, 76, 275–285.
Finn, D.S., Encalada, A.C. & Hampel, H. (2016) Genetic isolation among mountains but not between stream types in a tropical high-altitude mayfly. Freshwater Biology, 61 (5), 702–714. https://doi.org/10.1111/fwb.12740
Gattolliat, J.L., Rutschmann, S., Monaghan, M. & Sartori, M. (2018) From molecular hypotheses to valid species: Description of three species of Baetis (Ephemeroptera: Baetidae) from the Canary Islands. Arthropod Systematics and Phylogeny, 76 (3), 509–528.
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.
Hebert, P., Cywinska, A., Ball, S.L. & Dewaard, J. (2003) Biological identification through DNA barcodes. Proceedings of the Royal Society of London B, 270 (1512), 313–321. https://doi.org/10.1098/rspb.2002.2218
Jacobsen, D. & Marín, R. (2008) Bolivian Altiplano streams with low richness of macroinvertebrates and large diel fluctuations in temperature and dissolved oxygen. Aquatic Ecology, 42 (4), 643–656. https://doi.org/10.1007/s10452-007-9127-x
Jaume, D., Zapelloni, F., Pons, J., Juan, C. & Jurado-Rivera, J.A. (2021) The Hyalella species flock of Lake Titicaca (Crustacea: Amphipoda): perspectives and drawbacks of dna-based identification. Contributions to Zoology, 90 (4), 1–54 https://doi.org/10.1163/18759866-bja10021
Jurado-Rivera, J.A., Zapelloni, F., Pons, J., Juan, C. & Jaume, D. (2020) Morphological and molecular species boundaries in the Hyalella species flock of Lake Titicaca (Crustacea: Amphipoda). Contributions to Zoology, 89 (2020), 353–372. https://doi.org/10.1163/18759866-bja10004
Kroll, O., Hershler, R., Albrecht, C., Moreno, E., Apaza, R., Fuentealba, C., Wolff, C. & Wilke, T. (2012) The endemic gastropod fauna of Lake Titicaca: Correlation between molecular evolution and hydrographic history. Ecology and evolution, 2 (7), 1517–1530. https://doi.org/10.1002/ece3.280
Lugo-Ortiz, C.R. & McCafferty, W.P. (1999) Three New Genera of Small Minnow Mayflies (Insecta: Ephemeroptera: Baetidae) from the Andes and Patagonia. Studies on Neotropical Fauna and Environment, 34 (2), 88–104. https://doi.org/10.1076/snfe.34.2.88.2102
Lüssen, A., Falk, T.M. & Villwock, W. (2003) Phylogenetic patterns in populations of Chilean species of the genus Orestias (Teleostei: Cyprinodontidae): results of mitochondrial DNA analysis. Molecular Phylogenetics and Evolution, 29 (1), 151–160. https://doi.org/10.1016/s1055-7903(03)00077-0
Ministerio del Ambiente. (2014) Estado de la calidad ambiental de la cuenca del Lago Titicaca: Ámbito peruano. Ministerio del Ambiente. https://repositorio.ana.gob.pe/handle/20.500.12543/4549
Molina, C., Gibon, F.M. & Julio, P. (2008) Estructura de macroinvertebrados acuáticos en un río altoandino de la Cordillera Real, Bolivia: Variación anual y longitudinal en relación a factores ambientales. Ecología Aplicada, 7 (1), 105–116. https://doi.org/10.21704/rea.v7i1-2.365
Müller-Liebenau, J. (1971) Ephemeroptera (Insecta) von den Kanarischen Inseln. Gewässer und Abwässer, 50 (51), 7–40.
Needham, J. & Murphy, H. (1924) Neotropical Mayflies. Bulletin of the Lloyd Library, 24, 1–79.
Nieto, C. (2003) El Género Camelobaetidius (Ephemeroptera: Baetidae) en la Argentina. Acta Zoológica mexicana, 88, 233–255.
Nieto, C. (2004a) South American Baetidae (Ephemeroptera): A New Generic Synonymy. Studies on Neotropical Fauna and Environment, 39 (2), 95–101. https://doi.org/10.1080/01650520412331333747
Nieto, C. (2004b) The Genus Baetodes (Ephemeroptera: Baetidae) in South America with the description of new species from Argentina, Bolivia and Peru. Studies on Neotropical Fauna and Environment, 39 (1), 63–79. https://doi.org/10.1080/01650520412331270990
Nieto, C. (2008) The larvae of some species of Callibaetis Eaton (Ephemeroptera: Baetidae). Aquatic Insects, 30 (3), 229–243. https://doi.org/10.1080/01650420802010364
Nieto, C. (2010) Cladistic analysis of the family Baetidae (Insecta: Ephemeroptera) in South America. Systematic Entomology, 35 (3), 512–525. https://doi.org/10.1111/j.1365-3113.2010.00523.x
Ossa-López, P., Mathias, M. & Páez, F. (2018) Andesiops peruvianus (Ephemeroptera: Baetidae): a species complex based on molecular markers and morphology. Hydrobiologia, 805 (1), 351–364. https://doi.org/10.1007/s10750-017-3321-1
Polato, N., Gill, B., Shah, A., Gray, M., Casner, K., Barthelet, A., Messer, P., Simmons, M., Guayasamin, J., Encalada, A., Kondratieff, B., Thomas, S., Flecker, A., Ghalambor, C., Poff, N., Funk, W. & Zamudio, K. (2018) Narrow thermal tolerance and low dispersal drive higher speciation in tropical mountains. Proceedings of the National Academy of Sciences, 115 (49), 12471–12476. https://doi.org/10.1073/pnas.1809326115
Pons, J., Barraclough, T.G., Gómez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-Based Species Delimitation for the DNA Taxonomy of Undescribed Insects. Systematic Biology, 55 (4), 595–609. https://doi.org/10.1080/10635150600852011
Prosser, S., Martínez-Arce, A. & Elías-Gutiérrez, M. (2013) A new set of primers for COI amplification from freshwater microcrustaceans. Molecular Ecology Resources, 13 (6), 1151–1155. https://doi.org/10.1111/1755-0998.12132
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology, 67 (5), 901–904. https://doi.org/10.1093/sysbio/syy032
Ratnasingham, S. & Hebert, P. (2007) Bold: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes, 7 (3), 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
Raupach, M.J., Hannig, K., Morinière, J. & Hendrich, L. (2020) A DNA barcode library for ground beetles of Germany: The genus Pterostichus Bonelli, 1810 and allied taxa (Insecta, Coleoptera, Carabidae). ZooKeys, 980, 93–117. https://doi.org/10.3897/zookeys.980.55979
Remy, P. (1925) Contribution à l’étude de l’appareil respiratoire & de la respiration chez quelques invertebrés. Wagner, Nancy, 220 pp.
Ríos-Touma, B., Acosta, R. & Prat, N. (2014) The Andean Biotic Index (ABI): Revised tolerance to pollution values for macroinvertebrate families and index performance evaluation. Revista de Biología Tropical, 62 (2), 249–273. https://doi.org/10.15517/rbt.v62i0.15791
Sabando, M.C., Vila, I., Peñaloza, R. & Véliz, D. (2011) Contrasting population genetic structure of two widespread aquatic insects in the Chilean high-slope rivers. Marine & Freshwater Research, 62 (1), 1–10. https://doi.org/10.1071/MF10105
Suttinun, C., Gattolliat, J.L. & Boonsoong, B. (2020) Cymbalcloeon gen. nov., an incredible new mayfly genus (Ephemeroptera: Baetidae) from Thailand. PLoS ONE, 15 (10), e0240635. https://doi.org/10.1371/journal.pone.0240635
Traver, J. & Edmunds, G. (1968) A revision of the Baetidae with spatulate-clawed nymphs (Ephemeroptera). Pacific Insects, 10 (3–4), 629–667.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22 (22), 4673–4680. https://doi.org/10.1093/nar/22.22.4673
Ulmer, G. (1919)1920 Neue Ephemeropteren. Archiv für Naturgeschichte, 85 (11), 1–80.
Vilela, P., Falcao, F. & Hamasa, N. (2013) A New Genus and Species of Baetidae (Insecta: Ephemeroptera) from Brazil. Annales de Limnologie International Journal of Limnology, 49 (2013), 1–12. https://doi.org/10.1051/limn/2013033
Webb, J.M., Jacobus, L.M., Funk, D.H., Zhou, X., Kondratieff, B., Geraci, C.J., DeWalt, R.E., Baird, D.J., Richard, B., Phillips, I. & Hebert, P.D. (2012) A DNA Barcode Library for North American Ephemeroptera: Progress and Prospects. PLoS ONE, 7 (5), e38063. https://doi.org/10.1371/journal.pone.0038063
Wingfield, C.A. (1939) The Function of the Gills of Mayfly Nymphs from Different Habitats. Journal of Experimental Biology, 16 (3), 363–373. https://doi.org/10.1242/jeb.16.3.363
Zapelloni, F., Pons, J., Jurado-Rivera, J.A., Jaume, D. & Juan, C. (2021) Phylogenomics of the Hyalella amphipod species-flock of the Andean Altiplano. Scientific Reports, 11 (1), 1–14. https://doi.org/10.1038/s41598-020-79620-4
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29 (22), 2869–2876. https://doi.org/10.1093/bioinformatics/btt499