Abstract
The correct classification of organisms based on specific rules is essential in biological sciences. Traditionally, morphological characteristics such as size, shape, color, and anatomical structures have been used to identify and classify species. However, as consequence of the tremendous advances in molecular technologies during the last years, new approaches have become available for taxonomic research. Various modern high-throughput technologies allow the detailed characterization of the genome, proteome, metabolome as well as the morphology of an organism. Furthermore, the open access storage of such comprehensive data sets as part of an uprising digital cybertaxonomy enables highly fascinating digital dimensions for modern taxonomy, including the buildup of virtual collections as well as data sets for 3D printing techniques that can be used to replicate complete voucher specimens or at least important diagnostic characters. As a result of these advances, we are now able to document, describe, and identify species much more comprehensively than just a few years ago. In this review we provide an overview about the technical advances in taxonomic research in recent years and discuss their power and limitations.
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Akkari, N., Enghoff, H., & Metscher, B.D. (2015). A new dimension in documenting new species: High-detail imaging for myriapod taxonomy and first 3D cybertype of a new millipede species (Diplopoda, Julida, Julidae). Public Library of Science ONE, 10, e0135243.
Andújar, C., Arribas, P., Ruzicka, F., Crampton-Platt, A., Timmermans, M. J., & Vogler, A. (2015). Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics. Molecular Ecology, 24, 3603–3617.
Arienti, M., Antony, C., Wicker-Thomas, C., Delbecque, J. P., & Jallon, J. M. (2010). Ontogeny of Drosophila melanogaster female sex appeal and cuticular hydrocarbons. Integrative Zoology, 5, 272–282.
Asher, R. J., & Hofreiter, M. (2006). Tenrec phylogeny and the noninvasive extraction of nuclear DNA. Systematic Biology, 55, 181–194.
Ashton, L., Lau, K., Winder, C. L., & Goodacre, R. (2011). Raman spectroscopy: lighting up the future of microbial identification. Future Microbiology, 6, 991–997.
Astrin, J., Zhou, X., & Misof, B. (2013). The importance of biobanking in molecular taxonomy, with proposed definitions for vouchers in a molecular context. ZooKeys, 365, 67–70.
Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., et al. (2008). Rapid SNP discovery and genetic mapping using RAD markers. Public Library of Science ONE, 3, e3376.
Balke, M., Schmidt, S., Hausmann, A., Toussaint, E. F. A., Bergsten, J., Buffington, M., et al. (2013). Biodiversity into your hands—a call for a virtual global natural history “metacollection”. Frontiers in Zoology, 10, 55.
Bi, K., Linderoth, T., Vanderpool, D., Good, J. M., Nielsen, R., & Moritz, C. (2013). Unlocking the vault: next-generation museum population genomics. Molecular Ecology, 22, 6018–6032.
Blacket, M. J., Semeraro, L., & Malipatil, M. B. (2012). Barcoding Queensland fruit flies (Bactrocera tryoni): impediments and improvements. Molecular Ecology Resources, 12, 428–436.
Boistel, R., Swoger, J., Kržic, U., Fernandez, F., Gillet, B., & Reynaud, E. G. (2011). The future of three-dimensional microscopic imaging in marine biology. Marine Ecology, 32, 438–452.
Brooker, A. J., Shinn, A. P., & Bron, J. E. (2012). Use of laser scanning confocal microscopy for morphological taxonomy and the potential for digital type specimens (e-types). Aquatic Biology, 14, 165–173.
Bucklin, A., Steinke, D., & Blanco-Bercial, L. (2011). DNA barcoding of marine Metazoa. Annual Review of Marine Science, 3, 471–508.
Butcher, B. A., Smith, M. A., Sharkey, M. J., & Quicke, D. L. J. (2012). A turbo-taxonomic study of Thai Aleiodes (Aleiodes) and Aleiodes (Arcaleiodes) (Hymenoptera: Braconidae: Rogadinae) based largely on COI barcoded specimens, with rapid descriptions of 179 new species. Zootaxa, 3457, 1–232.
Cameron, S., Rubinoff, D., & Will, K. (2006). Who will actually use DNA barcoding and what will it cost? Systematic Biology, 55, 844–847.
Cappelini, E., Gentry, A., Palkopoulou, E., Ishida, Y., Cram, D., Roos, A.-M., et al. (2014). Resolution of the type material of the Asian elephant, Elephas maximus Linnaeus, 1758 (Proboscidea, Elephantidae). Zoological Journal of the Linnean Society, 170, 222–232.
Carstens, B. C., Pelletier, T. A., Reid, N. M., & Satler, J. D. (2013). How to fail at species delimitation. Molecular Ecology, 22, 4369–4383.
Chang, S. C., Chan, T. Y., & Ahyong, S. T. (2014). Two new species of the rare lobster genus Thaumastocheles Wood-Mason, 1874 (Reptantia: Nephropidae) discovered from recent deep-sea expeditions in the Indo-West Pacific. Journal of Crustacean Biology, 34, 107–122.
Chen, H.-N., Høeg, J. T., & Chan, B. K. K. (2013). Morphometric and molecular identification of individual barnacle cyprids from wild plankton: an approach to detecting fouling and invasive barnacle species. Biofouling, 29, 133–145.
Chun, J., & Rainey, F. A. (2014). Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. International Journal of Systematic and Evolutionary Microbiology, 64, 316–324.
Cochrane, G., Cook, C. E., & Birney, E. (2012). The future of DNA sequence archiving. GigaScience, 1, 2.
Cook, L. G., Edwards, R. D., Crisp, M. D., & Hardy, N. B. (2010). Need morphology always be required for new species descriptions? Invertebrate Systematics, 24, 322–326.
Correa, M. C. G., Germain, J.-F., Malausa, T., & Zaviezo, T. (2012). Molecular and morphological characterization of mealybugs (Hemiptera: Pseudococcidae) from Chilean vineyards. Bulletin of Entomological Research, 102, 524–530.
Corthals, A., & DeSalle, R. (2005). An application of tissue and DNA banking for genomics and conservation: the Ambrose Monell Cryo-Collection (AMCC). Systematic Biology, 54, 819–823.
Costa-da-Silva, A., Marinotti, O., Ribeiro, J. M. C., Silva, M. C. P., Lopes, A. R., Barros, M. S., et al. (2014). Transcriptome sequencing and developmental regulation of gene expression in Anopheles aquasalis. Public Library of Science ONE, 8, e3005.
Cozzuol, M. A., Clozato, C. L., Holanda, E. C., Rondrigues, F. H. G., Nienow, S., de Thoisy, B., et al. (2013). A new species of tapir from Amazon. Journal of Mammalogy, 94, 1331–1345.
Crampton-Platt, A., Timmermans, M. J. T. N., Gimmel, M. L., Kutty, S. N., Cockerill, T. D., Khen, C. V., et al. (2015). Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a Bornean rainforest sample. Molecular Biology and Evolution, 32, 2302–2316.
Cristescu, M. E. (2014). From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends in Ecology and Evolution, 29, 566–571.
Cvačka, J., Jiroŝ, P., Ŝobotník, J., Hanus, R., & Svatoŝ, A. (2006). Analysis of insect cuticular hydrocarbons using matrix-assisted laser desorption/ionization mass spectrometry. Journal of Chemical Ecology, 32, 409–434.
Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
De Bruyne, K., Slabbinck, B., Waegeman, W., Vauterin, P., De Baets, B., & Vandamme, P. (2011). Bacterial species identification from MALDI-TOF mass spectra through data analysis and machine learning. Systematic and Applied Microbiology, 34, 20–29.
Diz, A. P., Martínez-Fernández, M., & Rolán-Alvarez, E. (2012). Proteomics in evolutionary ecology: linking the genotype with the phenotype. Molecular Ecology, 21, 1060–1080.
Dufresne, F., & Jeffery, N. (2011). A guided tour of large genome size in animals: what we know and where we are heading. Chromosome Research, 19, 925–938.
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., et al. (2008). Broad phylogenetic sampling improves resolution of the animal tree of life. Nature, 452, 745–749.
Dupuis, J. R., Roe, A. R., & Sperling, F. A. H. (2012). Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Molecular Ecology, 21, 4422–4436.
Eaton, M. J., Meyers, G. L., Kolokotronis, S.-O., Leslie, M. S., Martin, A. P., & Amato, G. (2010). Barcoding bushmeat: molecular identification of Central African and South American harvested vertebrates. Conservation Genetics, 11, 1389–1404.
Eichner, C., Frost, P., Dysvik, B., Jonassen, I., Kristiansen, B., & Nilsen, F. (2011). Salmon louse (Lepeophtheirus salmonis) transcriptomes during post molting maturation and egg production, revealed using EST-sequencing and microarray analysis. BMC Genomics, 9, 126.
Enghoff, H. (2009). What is taxonomy?—an overview with myriapodological examples. Soil Organisms, 81, 441–451.
Engstrand, R. C., Tovar, J. C., Cibrián-Jaramillo, A., & Kolokotronis, S.-O. (2010). Genetic variation in avocado stem weevils Copturus aguacatae (Coleoptera: Curculionidae) in Mexico. Mitochondrial DNA, 21, 38–43.
Erpenbeck, D., Hooper, J. N. A., Bonnard, I., Sutcliffe, P., Chandra, M., Perio, P., et al. (2012). Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites. Marine Biology, 159, 1119–1127.
Faulwetter, S., Vasileiadou, A., Kouratoras, M., Dailianis, T., & Arvanitidis, C. (2013). Micro-computed tomography: introducing new dimensions to taxonomy. ZooKeys, 263, 1–45.
Feltens, R., Görner, R., Kalkhof, S., Gröger-Arndt, H., & von Bergen, M. (2010). Discrimination of different species from the genus Drosophila by intact protein profiling using matrix-assisted laser desorption ionization mass spectrometry. BMC Evolutionary Biology, 10, 95.
Ferguson, B., Street, S. L., Wright, H., Pearson, C., Jia, Y., Thompson, S. L., et al. (2007). Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genomics, 8, 43.
Fournier, P.-E., Drancourt, M., Colson, P., Rolain, J.-M., La Scola, B., & Raoult, D. (2013). Modern clinical microbiology: new challenges and solutions. Nature Reviews Microbiology, 11, 574–585.
Frentiu, F. D., & Chenoweth, S. F. (2010). Clines in cuticular hydrocarbons in two Drosophila species with independent population histories. Evolution, 64, 1784–1794.
Frisvad, J. C., Andersen, B., & Thrane, U. (2008). The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycological Research, 112, 231–240.
Fujita, M. K., Leaché, A. D., Burbrink, F. T., McGuire, J. A., & Moritz, C. (2012). Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology and Evolution, 27, 480–488.
Gonçalves, P. F. M., Oliveira-Marques, A. R., Matsumoto, T. E., & Miyaki, C. Y. (2015). DNA barcoding identifies illegal parrot trade. Journal of Heredity, 106, 560–564.
Gotelli, N. J., Ellison, A. M., & Ballif, B. A. (2012). Environmental proteomics, biodiversity studies, and food-web structure. Trends in Ecology and Evolution, 27, 436–442.
Guillem, R. M., Drijfhout, F. P., & Martin, S. J. (2012). Using chemo-taxonomy of host ants to help conserve the large blue butterfly. Biological Conservation, 148, 39–43.
Guschanski, K., Krause, J., Sawyer, S., Valente, L. M., Bailey, S., Finstermeier, K., et al. (2013). Next-generation museomics disentangles one of the largest primate radiations. Systematic Biology, 62, 539–554.
Hanai, T. (1999). HPLC: a practical guide (RSC chromatography monographs). Letchworth: The Royal Society of Chemistry.
Handschuh, S., Baeumler, N., Schwaha, T., & Ruthensteiner, B. (2013). A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario. Frontiers in Zoology, 10, 44.
Haus, T., Akom, E., Agwanda, B., Hofreiter, M., Roos, C., & Zinner, D. (2013). Mitochondrial diversity and distribution of African green monkeys (Chlorocebus Gray, 1870). American Journal of Primatology, 75, 350–360.
Hausmann, A., Godfray, H. C. J., Huemer, P., Mutanen, M., Rougerie, R., van Nieukerken, E. J., et al. (2013). Genetic patterns in European geometrid moths revealed by the Barcode Index Number (BIN system). Public Library of Science ONE, 8, e84518.
Haye, P. A., Segovia, N. I., Vera, R., Gallardo, M. D. A., & Gallardo-Escárate, C. (2012). Authentication of commercialized crab-meat in Chile using DNA barcoding. Food Control, 25, 239–244.
Hebert, P. D. N., Ratnasingham, S., & de Waard, J. R. (2003a). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270, S96–S99.
Hebert, P. D. N., Cywinska, A., Ball, S. L., & de Waard, J. R. (2003b). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270, 313–321.
Hebert, P. D. N., deWaard, J. R., Zakharov, E. V., Prosser, S. W. J., Sones, J. E., McKeown, J. T. A., et al. (2013). A DNA “Barcode Blitz”: rapid digitization and sequencing of a natural history collection. Public Library of Science ONE, 8, e68535.
Hendrich, L., Morinière, J., Haszprunar, G., Hebert, P. D. N., Hausmann, A., Köhler, F., et al. (2015). A comprehensive DNA barcode database for Central European beetles with a focus on Germany: adding more than 3500 identified species to BOLD. Molecular Ecology Resources, 15, 795–818.
Hrbek, T., da Silva, V. M. F., Dutra, N., Gravena, W., Martin, A. R., & Farias, I. P. (2014). A new species of river dolphin from Brazil or: how little do we know our biodiversity. Public Library of Science ONE, 9, e83623.
IISE (2011). State of observed species. Tempe, Arizona. International Institute for Species Exploration. Retrieved 2014-09-16 from http://www.esf.edu/species/SOS.htm
Ivanisěvić, J., Thomas, O. P., Lejeusne, C., Chevaldonné, P., & Pérez, T. (2011). Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics, 7, 289–304.
Ji, Y., Ashton, L., Pedley, S. M., Edwards, D. P., Tang, Y., Nakamura, A., et al. (2013). Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Ecology Letters, 16, 1245–1257.
Jónsson, H., Schubert, M., Seguin-Orlando, A., Ginolhac, A., Peterson, L., Fumagalli, M., et al. (2014). Speciation with gene flow in equids despite extensive chromosomal plasticity. Proceedings of the National Academy of Sciences of the United States of America, 111, 18655–18660.
Karas, M., & Hillenkamp, F. (1988 ). Laser desorption ionization of proteins with molecular masses exceeding 10000 daltons. Analytical Chemistry, 60, 2299–2303.
Karr, T. L. (2008). Application of proteomics to ecology and population biology. Heredity, 100, 200–206.
Kather, R., & Martin, S. J. (2012). Cuticular hydrocarbon profiles as a taxonomic tool: advantages, limitations and technical aspects. Physiological Entomology, 37, 25–32.
Kather, R., Drijfhout, F. P., & Martin, S. J. (2011). Task group differences in cuticular lipids in the honey bee Apis mellifera. Journal of Chemical Ecology, 37, 205–212.
Kaufmann, C., Ziegler, D., Schaffner, F., Carpenter, S., Pflüger, V., & Mathis, A. (2011). Evaluation of matrix-assisted laser desorption/ionization time off flight mass spectrometry for characterization of Culicoides nubeculosus biting midges. Medical and Veterinary Entomology, 25, 32–38.
Khalaji-Pirbalouty, V., & Raupach, M. J. (2014). A new species of Cymodoce Leach, 1814 (Crustacea: Isopoda: Sphaeromatidae) based on morphological and molecular data, with a key to the Northern Indian Ocean species. Zootaxa, 3826, 230–254.
Kircher, M., & Kelso, J. (2010). High-throughput DNA sequencing—concepts and limitations. BioEssays, 32, 524–536.
Kron, P., Suda, J., & Husband, B. C. (2007). Application of flow cytometry to evolutionary and population biology. Annual Review of Ecology, Evolution, and Systematics, 38, 847–876.
Laakmann, S., Gerdts, G., Erler, R., Knebelsberger, T., Martínez Arbízu, P., & Raupach, M. J. (2013). Comparison of molecular species identification for North Sea calanoid copepods (Crustacea) using proteome fingerprints and DNA sequences. Molecular Ecology Resources, 13, 862–876.
Lamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., et al. (2015). Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature, 518, 371–375.
Leaché, A. D., Fujita, M. K., Minin, V. N., & Bouckaert, R. R. (2014). Species delimitation using genome-wide SNP data. Systematic Biology, 63, 534–542.
Lenihan, J., Kvist, S., Fernández, S., Giribret, G., & Ziegler, A. (2014). A dataset comprising four microcomputed tomography scans of freshly fixed and museum earthworm specimens. GigaScience, 3, 6.
Leray, M., & Knowlton, N. (2015). DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proceedings of the National Academy of Sciences of the United States of America, 112, 2076–2081.
Liang, D., & Silverman, J. (2000). ‘You are what you eat’: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften, 87, 412–416.
Liedigk, R., Kolleck, J., Böker, K. O., Meeijard, E., Md-Zain, B. M., Abdul-Latiff, M. A. B., et al. (2015). Mitogenomic phylogeny of the common long-tailed macaque (Macaca fascicularis fascicularis). BMC Genomics, 16, 222.
Lockey, K. H. (1988). Lipids of the insect cuticle: origin, composition and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 89, 595–645.
Lu, G.-H., Chan, K., Liang, Y.-Z., Leung, K., Chan, C.-L., Jiang, Z.-H., et al. (2005). Development of high-performance liquid chromatographic fingerprints for distinguishing Chinese Angelica from related umbelliferae herbs. Journal of Chromatography A, 1073, 383–392.
Mardis, E. R. (2013). Next-generation sequencing platforms. Annual Review of Analytical Chemistry, 6, 287–303.
Martin, S. J., Helantera, H., & Drijfhout, F. P. (2008). Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biological Journal of the Linnean Society, 95, 131–140.
May, R. R., & Harvey, P. H. (2009). Species uncertainties. Science, 323, 687.
Mayagaya, V. S., Michel, K., Benedict, M. Q., Killeen, G. F., Wirtz, R. A., Ferguson, H. M., et al. (2009). Non-destructive determination of age and species of Anopheles gambiae s.l. using near-infrared spectroscopy. The American Journal of Tropical Medicine and Hygiene, 81, 622–630.
Mazzeo, M. F., de Giulio, B., Guerriero, G., Ciarcia, G., Malorni, A., Russo, G. L., et al. (2008). Fish authentication by MALDI-TOF mass spectrometry. Journal of Agricultural and Food Chemistry, 56, 11071–11076.
Miller, J., Dikow, T., Agosti, D., Sautter, G., Catapano, T., Penev, L., et al. (2012). From taxonomic literature to cybertaxonomic content. BMC Biology, 10, 87.
Miller, J. A., Miller, J. H., Pham, D.-S., & Beentjes, K. K. (2014). Cyberdiversity: Improving the informatic value of diverse tropical arthropod inventories. Public Library of Science ONE, 9, e115750.
Minelli, A. (2013). Zoological nomenclature in the digital era. Frontiers in Zoology, 10, 4.
Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., et al. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science, 346, 763–767.
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B., & Worm, B. (2011). How many species are there on Earth and in the ocean? Public Library of Science Biology, 9, e1001127.
Nadeau, N. J., Martin, S. H., Kozak, K. M., Salazar, C., Dasmahapatra, K., Davey, J. W., et al. (2013). Genome-wide patterns of divergence and gene flow across a butterfly radiation. Molecular Ecology, 22, 814–826.
Nagy, Z. T., Sonet, G., Glaw, F., & Vences, M. (2012). First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. Public Library of Science ONE, 7, e34506.
Nelson, L. A., Wallman, J. F., & Dowton, M. (2007). Using COI barcodes to identify forensically and medically important blowflies. Medical and Veterinary Entomology, 21, 44–52.
Nicholson, S. J., & Puterka, G. J. (2014). Variation in the salivary proteomes of differently virulent green bug (Schizaphis graminum Rondani) biotypes. Journal of Proteomics, 105, 186–203.
Oakley, T. H., Wolfe, J. M., Lindgren, A. R., & Zaharoff, A. K. (2012). Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement, and pancrustacean phylogeny. Molecular Biology and Evolution, 30, 215–233.
Oetjen, J., Veselkov, K., Watrous, J., McKenzie, J. S., Becker, M., Hauberg-Lotte, L., et al. (2015). Benchmark datasets for 3D MALDI- and DESI-imaging mass spectrometry. GigaScience, 4, 20.
Orgiazzi, A., Dunbar, M. B., Panagos, P., de Groot, G. A., & Lemanceau, P. (2015). Soil biodiversity and DNA barcodes: opportunities and challenges. Soil Biology & Biochemistry, 80, 244–250.
Padial, J. M., Miralles, A., de la Riva, I., & Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7, 16.
Pante, E., Abdelkrim, J., Viricel, A., Gey, D., France, S. C., Boisselier, M. C., et al. (2015). Use of RAD sequencing for delimiting species. Heredity, 114, 450–459.
Papadopoulou, A., Taberlet, P., & Zinger, L. (2015). Metagenome skimming for phylogenetic community ecology: a new era in biodiversity research. Molecular Ecology, 24, 3515–3517.
Pasquini, C. (2003). Near infrared spectroscopy: fundamentals practical aspects and analytical applications. Journal of the Brazilian Chemical Society, 14, 138–219.
Perelman, P., Johnson, W. E., Roos, C., Seuanez, H. N., Horvath, J. E., Moreira, M. A. M., et al. (2011). A molecular phylogeny of living primates. Public Library of Science Genetics, 7, e1001342.
Pettersen, R., Johnsen, G., Bruheim, P., & Andreassen, T. (2014). Development of hyperspectral imaging as a bio-optical taxonomic tool for pigmented marine organisms. Organisms, Diversity and Evolution, 14, 237–246.
Pilgrim, E. M., & Darling, J. A. (2010). Genetic diversity in two introduced biofouling amphipods (Ampithoe valida & Jassa marmorata) along the Pacific North American coast: investigation into molecular identification and cryptic diversity. Diversity and Distributions, 16, 827–839.
Poelstra, J. W., Vijay, N., Bossu, C. M., Lantz, H., Ryll, B., Müller, I., et al. (2014). The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science, 344, 1410–1414.
Polaszek, A., Agosti, D., Alonso-Zarazaga, M., Beccaloni, G., de Place Bjørn, P., Bouchet, P., et al. (2005). A universal register for animal names. Nature, 437, 477.
Pop, M., & Salzberg, S. L. (2008). Bioinformatics challenges of new sequencing technology. Trends in Genetics, 24, 142–149.
Puillandre, N., Reto, S., Philippe, F., Estelle, B., Frédéric, P., Audrey, R., et al. (2014). When everything converges: Integrative taxonomy with shell, DNA and venomic data reveals Conus conco, a new species of cone snails (Gastropoda: Conoidea). Molecular Phylogenetics and Evolution, 80, 186–192.
Rasmussen, R. S., Morrissey, M. T., & Hebert, P. D. N. (2013). DNA barcoding of commercially important salmon and trout species (Oncorhynchus and Salmo) from North America. Journal of Agricultural and Food Chemistry, 57, 8379–8385.
Raupach, M. J., Hendrich, L., Küchler, S. M., Deister, F., Morinière, J., & Gossner, M. M. (2014). Building-up of a DNA barcode library for True Bugs (Insecta: Hemiptera: Heteroptera) of Germany reveals taxonomic uncertainties and surprises. Public Library of Sciences ONE, 9, e106940.
Rendón-Anaya, M., Delaye, L., Possani, L. D., & Herrera-Estrella, A. (2012). Global transcriptome analysis of the scorpion Centruroides noxius: new toxin families and evolutionary insights from an ancestral scorpion species. Public Library of Sciences ONE, 7, e43331.
Riccardi, N., Lucini, L., Benagli, C., Welker, M., Wicht, B., & Tonolla, M. (2012). Potential of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) for the identification of freshwater zooplankton: a pilot study with three Eudiaptomus (Copepoda: Diaptomidae) species. Journal of Plankton Research, 34, 1–9.
Richter, M., & Rosselló-Móra, R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences of the United States of America, 106, 19126–19131.
Riedel, A., Sagata, K., Suhardjono, Y. R., Tänzler, R., & Balke, M. (2013a). Integrative taxonomy on the fast track—towards more sustainability in biodiversity research. Frontiers in Zoology, 10, 15.
Riedel, A., Sagata, K., Surbakti, S., Tänzler, R., & Balke, M. (2013b). One hundred and one new species of Trigonopterus weevils from New Guinea. ZooKeys, 280, 1–150.
Riesgo, A., Andrade, S. C. S., Sharma, P. P., Novo, M., Pérez-Porro, A. R., Vahtera, V., et al. (2012). Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Frontiers in Zoology, 9, 33.
Rodríguez-Fernández, J. I., de Carvalho, C. J. B., Pasquini, C., de Lima, K. M. G., Moura, M. O., & Arízaga, G. G. C. (2011). Barcoding without DNA? Species identification using near infrared spectroscopy. Zootaxa, 2933, 46–54.
Romiguier, J., Gayral, P., Ballenghien, M., Bernard, A., Cahais, A., Chenuil, A., et al. (2014). Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515, 261–263.
Roos, C., Nadler, T., & Walter, L. (2008). Mitochondrial phylogeny, taxonomy and biogeography of the silvered langur species group (Trachypithecus cristatus). Molecular Phylogenetics and Evolution, 47, 629–636.
Roos, C., Zinner, D., Kubatko, L. S., Schwarz, C., Yang, M., Meyer, D., et al. (2011). Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys. BMC Evolutionary Biology, 11, 77.
Rosenberg, M. S. (2012). Contextual cross-referencing of species names for fiddler crabs (Genus: Uca): an experiment in cyber-taxonomy. Public Library of Science ONE, 9, e101704.
Rowe, K. C., Singhal, S., MacManes, M. D., Ayroles, J. F., Morelli, T. L., Rubidge, E. M., et al. (2011). Museum genomics: low-cast and high accuracy genetic data from historical specimens. Molecular Ecology Resources, 11, 1082–1092.
Sauer, S., & Kliem, M. (2010). Mass spectrometry tools for the classification and identification of bacteria. Nature Reviews Microbiology, 8, 74–82.
Savolainen, P., & Reeves, G. (2004). A plea for DNA banking. Science, 304, 1445.
Schilthuizen, M., Scholte, C., van Wijk, R. E. J., Doimmershuijzen, J., van der Horst, D., Meijer zu Schlochtern, M., et al. (2011). Using DNA-barcoding to make the necrobiont beetle family Cholevidae accessible for forensic entomology. Forensic Science International, 210, 91–95.
Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., & Crozier, R. H. (2010). Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology, 55, 421–438.
Schneider, M. V., & Orchard, S. (2011). Omics technologies, data and bioinformatic principles. Methods in Molecular Biology, 719, 3–30.
Schunter, C., Vollmer, S. V., Macpherson, E., & Pascual, M. (2014). Transcriptome analyses and differential gene expression in a non-model fish species with alternative mating tactics. BMC Genomics, 15, 167.
Sehrawat, N., & Gakhar, S. K. (2014). Mosquito proteomics: present and future perspective. Research in Biotechnology, 5, 25–33.
Serrano, W., Amann, R., Rosselló-Mora, R., & Fischer, U. (2010). Evaluation of the use of multilocus sequence analysis (MLSA) to resolve taxonomic conflicts within the genus Marichromatium. Systematic and Applied Microbiology, 33, 116–121.
Sherwin, W. B., Frommer, M., Sved, J. A., Raphael, K. A., Oakeshott, J. G., Shearman, D. C. A., et al. (2015). Tracking invasion and invasiveness in Queensland fruit flies: from classical genetics to ‘omics’. Current Zoology, 61, 477–487.
Shevtsova, E., Hansson, C., Janzen, D. H., & Kjærandsen, J. (2011). Stable structural color patterns displayed on transparent insect wings. Proceedings of the National Academy of Sciences of the United States of America, 108, 668–673.
Shipway, J. R., Borges, L. M. S., Müller, J., & Cragg, S. M. (2014). The broadcast spawning Caribbean shipworm, Teredothyra dominicensis (Bivalvia, Teredinidae), has invaded and become established in the eastern Mediterranean Sea. Biological Invasions, 16, 2037–2048.
Skoog, D. A., Holler, F. J., & Crouch, S. R. (2006). Principles of Instrumental Analysis. Boston: Cengage Learning.
Soldati, L., Kergoat, G. J., Clamens, A.-L., Jourdan, H., Jabbour-Zahab, R., & Condamine, F. L. (2014). Integrative taxonomy of New Caledonian beetles: species delimitation and definition of the Uloma isoceroides species group (Coleoptera, Tenebrionidae, Ulomini), with the description of four new species. ZooKeys, 415, 133–167.
Sombke, A., Lipke, E., Michalik, P., Uhl, G., & Harzsch, S. (2015). Potential and limitations of X-ray micro-computed tomography in arthropod neuroanatomy: a methodological and comparative survey. The Journal of Comparative Neurology, 523, 1281–1295.
Spelda, J., Reip, H. S., Oliveira-Biener, U., & Melzer, R. R. (2011). Barcoding Fauna Bavarica—a contribution to DNA sequence-based identifications of centipedes and millipedes (Chilopoda, Diplopoda). ZooKeys, 156, 123–139.
Stoev, P., Komerički, A., Akkari, N., Liu, S., Zhou, X., Weigand, A. M., et al. (2013). Eupolybothrus cavernicolus Komerički & Stoev sp. n. (Chilopoda: Lithobiomorpha: Lithobiidae): the first eukaryotic species description combining transcriptomic, DNA barcoding and micro-CT imaging data. Biodiversity Data Journal, 1, e1013.
Struck, T. H., Paul, C., Hill, N., Hartmann, S., Hösel, C., Kube, M., et al. (2011). Phylogenetic analyses unravel annelid evolution. Nature, 471, 95–98.
Strutzenberger, P., Brehm, G., & Fiedler, K. (2013). DNA barcode sequencing from old type specimens as a tool in taxonomy: a case study in diverse Eois (Lepidoptera: Geometridae). Public Library of Science ONE, 7, e49710.
Summers, M. M., Al-Hakim, I. I., & Rouse, G. W. (2014). Turbo-taxonomy: 21 new species of Myzostomida (Annelida). Zootaxa, 3873, 301–344.
Tang, M., Tan, M., Meng, G., Yang, S., Su, X., Liu, S., et al. (2014). Multiplex sequencing of pooled mitochondrial genomes—a crucial step toward biodiversity analysis using mito-genomics. Nucleic Acids Research, 42, e166.
Tang, M., Hardman, C. J., Ji, Y., Meng, G., Liu, S., Tan, M., et al. (2015). High-throughput monitoring of wild bee diversity and abundance via mitogenomics. Methods in Ecology and Evolution. doi:10.1111/2041-210X.12416.
Taylor, H. R., & Harris, W. E. (2012). An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding. Molecular Ecology Resources, 12, 377–388.
Thinh, V. N., Mootnick, A. R., Thanh, V. N., Nadler, T., & Roos, C. (2010). A new species of crested gibbon, from the central Annamite mountain range. Vietnamese Journal of Primatology, 1, 1–12.
Thompson, C. C., Chimetto, L., Edwards, R. A., Swings, J., Stackebrandt, E., & Thompson, F. L. (2014). Microbial genomic taxonomy. BMC Genomics, 14, 913.
Valentini, A., Pompanon, F., & Taberlet, P. (2009). DNA barcoding for ecologists. Trends in Ecology and Evolution, 24, 110–117.
van Dijk, E. L., Auger, H., Jaszczyszyn, Y., & Thermes, C. (2014). Ten years of next-generation sequencing technologies. Trends in Genetics, 30, 418–426.
van Houdt, J. K. L., Breman, F. C., Virgilio, M., & de Meyer, M. (2010). Recovering full DNA barcodes from natural history collections of Tephritid fruitflies (Tephritidae, Diptera) using mini barcodes. Molecular Ecology Resources, 10, 459–465.
Villar, M., Popara, M., Mangold, A. J., & de la Fuente, J. (2014). Comparative proteomics for the characterization of the most relevant Amblyomma tick species as vectors of zoonotic pathogens worldwide. Journal of Proteomics, 105, 2014–2216.
Volta, P., Riccardi, N., Lauceri, R., & Tonolla, M. (2012). Discrimination of freshwater fish species by matrix-assisted laser desorption/ionization-time of flight mass spectrometry (MALDI-TOF MS): a pilot study. Journal of Limnology, 71, 164–169.
von Reumont, B. M., Jenner, R. A., Wills, M. A., DellÀmpio, E., Pass, G., Ebersberger, I., et al. (2012). Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia a possible sister group of Hexapoda. Molecular Biology and Evolution, 29, 1031–1045.
von Reumont, B. M., Blanke, A., Richter, S., Alvarez, F., Bleidorn, C., & Jenner, R. A. (2014). The first venomous crustacean revealed by transcriptomics and functional morphology: remipede venom glands express a unique toxin cocktail dominated by enzymes and a neurotoxin. Molecular Biology and Evolution, 31, 48–58.
Wang, X. P., Yu, L., Roos, C., Ting, N., Chen, C. P., Wang, J., et al. (2012). Phylogenetic relationships among the colobine monkeys revisited: new insights from analyses of complete mt genomes and 44 nuclear non-coding markers. Public Library of Science ONE, 7, e36274.
Weis, A., Meyer, R., Dietz, L., Dömel, J. S., Leese, F., & Melzer, R. R. (2014). Pallenopsis patagonica (Hoek, 1881)—a species complex revealed by morphology and DNA barcoding, with description of a new species of Pallenopsis Wilson, 1881. Zoological Journal of the Linnean Society, 170, 110–131.
Welker, M., & Moore, E. R. B. (2011). Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Systematic and Applied Microbiology, 34, 2–11.
Wenning, M., & Scherer, S. (2013). Identification of microorganisms by FTIR spectroscopy: perspectives and limitations of the method. Applied Microbiology and Biotechnology, 97, 7111–7120.
Wheeler, Q. D., & Valdecasas, A. G. (2010). Cybertaxonomy and ecology. Nature Education Knowledge, 3, 6.
Wheeler, Q. D., Bourgoin, T., Coddington, J., Gostony, T., Hamilton, A., Larimer, R., et al. (2012). Nomenclatural benchmarking: the roles of digital typification and telemicroscopy. ZooKeys, 209, 193–202.
Will, K. P., Mishler, P. D., & Wheeler, Q. D. (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54, 844–851.
Wilson, D., & Alewood, P. F. (2006). Taxonomy of Australian funnel-web spiders using rp-HPLC/ESI-MS profiling techniques. Toxicon, 47, 614–627.
Wilson, N. G., Maschek, J. A., & Baker, B. J. (2013). A species flock driven by predation? Secondary metabolites support diversification of slugs in Antarctica. Public Library of Sciences ONE, 8, e80277.
Yan, D., Luo, J. Y., Han, Y. M., Peng, C., Dong, X. P., Chen, S. L., et al. (2013). Forensic DNA barcoding and bio-response studies of animal horn products in traditional medicine. Public Library of Science ONE, 8, e55854.
Yang, Z., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America, 107, 9264–9269.
Zapata, M., Jeffrey, S. W., Wright, S. W., Rodríguez, F., Garrido, J. L., & Clementson, L. (2004). Photosynthetic pigments in 37 species (65 strains) of Haptophyta: implications for oceanography and chemotaxonomy. Marine Ecology Progress Series, 270, 83–102.
Zhou, X., Li, Y., Liu, S., Yang, Q., Su, X., Zhou, L., et al. (2013). Ultra-deep sequencing enables high-fidelity recovery of biodiversity bulk arthropod samples without PCR amplification. GiagaScience, 2, 4.
Ziegler, A., Ogurreck, M., Steinke, T., Beckmann, F., Prohaska, S., & Ziegler, A. (2010). Opportunities and challenges for digital morphology. Biology Direct, 5, 45.
Ziegler, A., Faber, C., Mueller, S., Nagelmann, N., & Schröder, L. (2014). A data set comprising 141 magnetic resonance imaging scans of 98 extant sea urchin species. GigaScience, 3, 31.
Zinner, D., Groeneveld, L. F., Keller, C., & Roos, C. (2009a). Mitochondrial phylogeography of baboons (Papio spp.)—indication for introgressive hybridization? BMC Evolutionary Biology, 9, 83.
Zinner, D., Arnold, M. L., & Roos, C. (2009b). Is the new primate genus Rungwecebus a baboon? Public Library of Science ONE, 4, e4859.
Acknowledgments
This review is in part based on the hearings and discussions within the working group “Taxonomic Research in the Era of OMICS Technologies” of the Leopoldina–Nationale Akademie der Wissenschaften (German National Academy of Sciences). We thank all participants of the working group for sharing their views and opinions. The English version of the statement “Challenges and Opportunities of Integrative Taxonomy for Research and Society” can be found here: www.leopoldina.org/en/taxonomy. We thank Terue Cristina Kihara for using the 3D model of the serolid isopod specimen, Karin Pointner for the permission to use the copepod image as well as Ortwin Bleich for his permission to use the ground beetle image taken from www.eurocarabidae.de. We also thank two anonymous reviewers for their helpful comments on the manuscript.
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Raupach, M.J., Amann, R., Wheeler, Q. et al. The application of “-omics” technologies for the classification and identification of animals. Org Divers Evol 16, 1–12 (2016). https://doi.org/10.1007/s13127-015-0234-6
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DOI: https://doi.org/10.1007/s13127-015-0234-6