Potential crypticity within two decapod (Crustacea) genera: Galathea Fabricius, 1793 and Eualus Thallwitz, 1891 suggested by integrative taxonomic approach

PDF (English) SUPPL FILE (English)
Publiée : Ιουν 20, 2022
DOI : https://doi.org/10.12681/mms.27733
SHEENA CONFORTI
ETH Zurich
https://orcid.org/0000-0002-0173-6170
FEDERICA COSTANTINI
Dipartimento di Scienze Biologiche, Geologiche e Ambientali & Centro Interdipartimentale di Ricerca per le Scienze Ambientali in Ravenna Università di Bologna, Campus di Ravenna, Ravenna, Italy
Résumé

Correct species identification and description are fundamental to understand the health status of marine ecosystems. The use of a single identification tool for species distinction may lead to species misidentifications, having major consequences for ecological studies. In the present research, we used an integrative taxonomic approach to identify benthic decapods belonging to the genera of Galathea Fabricius, 1793 and Eualus Thallwitz, 1891, collected in the Mediterranean Sea. 23 Galathea and 22 Eualus individuals were morphologically analyzed and sequenced at the mitochondrial COI gene to confirm their identity using the BOLD Identification Engine. Morphological identification revealed the presence of two Galathea and three Eualus species, while species delimitation based on DNA barcoding of COI sequences strongly suggested the presence of three Galathea and four Eualus species. Molecular analyses suggested the potential presence of two still undescribed species: one cryptic to Galathea squamifera and one cryptic to Galathea intermedia. Contrasting results obtained via morphological identification and the BOLD Identification Engine impeded the recognition of Eualus specimens and suggested misidentifications among BOLD reference records of Eualus cranchii, Eualus occultus, and Eualus pusiolus. These results demonstrated that morphological identification overlooks cryptic species and that misidentifications may occur, highlighting the importance of using an integrative approach to increase the current taxonomic knowledge of benthic invertebrates.

Article Details
  • Rubrique
  • Research Article

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Téléchargements
Les données relatives au téléchargement ne sont pas encore disponibles.
Biographie de l'auteur
SHEENA CONFORTI, ETH Zurich
Department of Environmental Microbiology, Eawag (Dübendorf, Switzerland) - PhD Candidate
Références
Akaike, H., 1973. Maximum likelihood identification of gaussian autoregressive moving average models. Biometrika, 60 (2), 255-265.
Anger, K., 2001. The biology of decapod crustacean larvae (Crustacean Issues 14). Aquaculture, 216 (1-4), 383-387.
Appeltans, W., Ahyong, S.T., Anderson, G., Angel, M.V., Artois, T. et al., 2012. The magnitude of global marine species diversity. Current Biology, 22 (23), 2189-2202.
Bate, C.S., 1859. On the importance of an examination of the structure of the integument of Crustacea in the determination of doubtful species - Application to the genus Galathea, with the description of a new species of that genus. Journal of the Proceedings of the Linnean Society. Zoology, 3, 1-4.
Bayha, K.M., Collins, A.G, Gaffney, P.M., 2017. Multigene phylogeny of the scyphozoan jellyfish family Pelagiidae reveals that the common U.S. Atlantic Sea nettle comprises two distinct species (Chrysaora quinquecirrha and C. chesapeakei). PeerJ, 5, e3863.
Bianchi, C.N., Morri, C., 2000. Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin, 40 (5), 367-376.
Bilgin, R., Utkan, M.A., Kalkan, E., Karhan, S.Ü., Bekbolet, M., 2015. DNA barcoding of twelve shrimp species (Crustacea: Decapoda) from Turkish seas reveals cryptic diversity. Mediterranean Marine Science, 16 (1), 36-45.
Bishop, J.D.D., Roby, C., Yunnie, A.L.E., Wood, C.A., Lévêque, L. et al., 2013. The Southern Hemisphere ascidian Asterocarpa humilis is unrecognised but widely established in NW France and Great Britain. Biological Invasions, 15 (2), 253-260.
Bishop, J.D.D., Wood, C.A., Lévèque, L., Yunnie, A. L.E., Viard, F., 2015. Repeated rapid assessment surveys reveal contrasting trends in occupancy of marinas by non-indigenous species on opposite sides of the western English Channel. Marine Pollution Bulletin, 95 (2), 699-706.
Bortolus, A., 2008. Error Cascades in the Biological Sciences: The unwanted consequences of using bad taxonomy in ecology. AMBIO: A Journal of the Human Environment, 37 (2), 114-118.
Bouchet, P., 2006. The magnitude of marine biodiversity. p. 31-62. In: The exploration of marine biodiversity: scientific and technological challenges. Duarte, C. M. (Ed). Fundación BBVA, Bilbao.
Caputi, L., Andreakis, N., Mastrototaro, F., Cirino, P., Vassillo, M. et al., 2007. Cryptic speciation in a model invertebrate chordate. Proceedings of the National Academy of Sciences of the United States of America, 104 (22), 9364-9369.
Chenuil, A., Cahill, A. E., Délémontey, N., Du Salliant du Luc, E., Fanton, H., 2019. Problems and Questions Posed by Cryptic Species. A Framework to Guide Future Studies. p. 77-106. In: From Assessing to Conserving Biodiversity. History, Philosophy and Theory of the Life Sciences, vol 24.
Casetta, E., Marques da Silva, J., Vecchi, D. (Eds). Springer, Cham. Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Sayers, E.W., 2015. GenBank. Nucleic Acids Research, 44 (D1), D67-D72.
Colloca, F., Cardinale, M., Belluscio, A., Ardizzone, G., 2003. Pattern of distribution and diversity of demersal assemblages in the central Mediterranean Sea. Estuarine, Coastal and Shelf Science, 56 (3-4), 469-480.
Company, J.B., Puig, P., Sardà, F., Palanques, A., Latasa, M. et al., 2008. Climate influence on deep sea populations. PLoS ONE, 3 (1), e1431.
Costello, M.J., Wilson, S., Houlding, B., 2012. Predicting total global species richness using rates of species description and estimates of taxonomic effort. Systematic Biology, 61 (5), 871-883.
Dayrat, B., 2005. Towards integrative taxonomy. Biological Journal of the Linnean Society, 85 (3), 407-415.
De Queiroz, K., 2007. Species concepts and species delimitation. Systematic biology, 56 (6), 879-886.
Dewalt, R.E., 2011. DNA barcoding: A taxonomic point of view. Journal of the North American Benthological Society, 30 (1), 174-181.
D’Udekem-d’Acoz, C., Wirtz, P., 2002. Observations on some interesting coastal Crustacea Decapoda from the Azores, with a key to the genus Eualus Thallwitz, 1892 in the Northeastern Atlantic and the Mediterranean. Arquipelago. Life and Marine Science, 19A, 67-84.
Embleton, R., 1836. List of Malacostraca Podophthalmata, found on the coasts of Berwickshire and North Durham, years 1832-1841. History of the Berwickshire Naturalists’ Club, 1, 69-72.
Ensing, D.J., Moffat, C.E., Pither, J., 2013. Taxonomic identification errors generate misleading ecological niche model predictions of an invasive hawkweed. Botany, 91 (3), 137- 147.
Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39 (4), 783-791.
Fukami, K., Tateno, Y., 1989. On the maximum likelihood method for estimating molecular trees: uniqueness of the likelihood point. Journal of molecular evolution, 28 (5), 460-464.
Geller, J., Meyer, C., Parker, M., Hawk, H. et al., 2013. Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources, 13 (5), 851-861.
Gollasch, S., 2006. Overview on introduced aquatic species in European navigational and adjacent waters. Helgoland Marine Research, 60, 84-89.
Goulletquer, P., Gros, P., Boeuf, G., Weber, J., 2014. Biodiversity in the marine environment. Springer, Cham, 198 pp.
Guijarro, B., Massutí, E., Moranta, J., Cartes, J.E., 2009. Short spatio-temporal variations in the population dynamics and biology of the deep-water rose shrimp Parapenaeus longirostris (Decapoda: Crustacea) in the western Mediterranean. Scientia Marina, 73 (1), 183-197.
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.
Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, C.V., Micheli, F. et al., 2008. A global map of human impact on marine ecosystems. Science, 319 (5865), 948-952.
Harrington, B., Engelen, J., 2004. Inkscape. Software available at http://www.Inkscape.org. Hasegawa, M., Kishino H., Yano T.A., 1985. Dating of the human- ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22 (2), 160-174.
Hebert, P.D.N., Cywinska, A., Ball, S.L., deWaard, J.R., 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270 (1512), 313-321.
Hillis, D.M., Moritz, C., 1990. Molecular systematics. Science, 250 (4983), 1022-1023.
Jukes, T.H., Cantor, C.R., 1969. Evolution of Protein Molecules. p. 21-132. In: Mammalian Protein Metabolism. Munro, H. N., (Ed). Academic Press, New York.
Kemp, S., 1925. Notes on Crustacea Decapoda in the Indian Museum. XVII On various Caridea. Records of the Indian Museum, 27, 249-342.
Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111-120.
Knowlton, N., 1986. Cryptic and sibling species among the decapod crustacea. Journal of Crustacean Biology, 6 (3), 356-363.
Kronenberger, K., Türkay, M., 2003. A population study of Galathea intermedia (Crustacea: Decapoda: Anomura) in the German Bight. Journal of the Marine Biological Association of the United Kingdom, 83 (1), 133-141.
Krøyer, H., 1841. Fire nye arter af slægten Cuma Edw. Naturhistorisk Tidsskrift Ser II, 3(6), 503-535.
Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular biology and evolution, 33 (7), 1870-1874. Leach, W.E., 1813-1815. Crustaceology. 7(1): 383–384 [1813], 7(2), 385–437, 765–766 [1814], 9(1), Pl. CCXXI [1815]. In: The Edinburgh Encyclopaedia. Brewster, D. (Ed). Balfour, Edinburgh. Lebour, M.V., 1936. Notes on the Plymouth species of Spirontocaris (Crustacea). Proceedings of the Zoological Society of London, 106 (1), 89-104, plates 1-7.
Lefébure, T., Douady, C. J., Gouy, M., Gibert, J., 2006. Relationship between morphological taxonomy and molecular divergence within Crustacea: Proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution, 40, 435-447.
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, 112 (7), 2076-2081.
Liljeborg, O., 1851. Norges Crustacéer. Ofversigt af Konglige Vetenskaps-Akademiens Förhandlingar, 8, 19-25. Linnaeus, C., 1761. Fauna Suecica sistens Animalia Sueciae Regni: Distributa per Classes, Ordines, Genera, Species, cum Differentiis Specierum, Synonymis Auctorum, Nominibus Incolarum, Locis Natalium, Descriptionibus insectorum. Editio altera, auctior. Stockholmiae, Stockhom, Sweden, 48, 1-578.
Machordom, A., Macpherson, E., 2004. Rapid radiation and cryptic speciation in squat lobsters of the genus Munida (Crustacea, Decapoda) and related genera in the South West Pacific: molecular and morphological evidence. Molecular Phylogenetics and Evolution, 33 (2), 259-279.
Macpherson, E., Robainas-Barcia, A., 2015. Species of the genus Galathea Fabricius, 1793 (Crustacea, Decapoda, Galatheidae) from the Indian and Pacific Oceans, with descriptions of 92 new species. Zootaxa, 3913 (1), 1-335.
May, R.M., 1992. Bottoms up for the oceans. Nature 357 (6376), 278-279.
Meier, R., Shiyang, K., Vaidya, G., Ng, P. K., 2006. DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Systematic Biology, 55 (5), 715-728.
Meiklejohn, K.A., Damaso, N., Robertson, J.M., 2019. Assessment of BOLD and GenBank - Their accuracy and reliability for the identification of biological materials. PloS ONE, 14 (6), e0217084. Milne Edwards, H., 1834-1840. Histoire Naturelle des Crustacés, Comprenant l´Anatomie, la Physiologie et la Classification de ces Animaux. Encyclopédique Roret, Paris, (I), i-xxxv + 1-468, (II), 1-532, (III), 1-638, Plates 1–42.
Molinari-Jobin, A., Kéry, M., Marboutin, E., Molinari, P., Koren, I. et al., 2012. Monitoring in the presence of species misidentification: the case of the Eurasian lynx in the Alps. Animal Conservation, 15 (3), 266-273.
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? PLoS Biology, 9 (8), 1-8.
Nye, V., Copley, J.T., Linse, K., 2013. A new species of Eualus Thallwitz, 1892 and new record of Lebbeus antarcticus (Hale, 1941) (Crustacea: Decapoda: Caridea: Hippolytidae) from the Scotia Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 92, 145-156.
Pante, E., Puillandre, N., Viricel, A., Arnaud-Haond, S., Aurelle, D. et al., 2015. Species are hypotheses: avoid connectivity assessments based on pillars of sand. Molecular Ecology, 24 (3), 525-544.
Paradis, E., 2010. pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics, 26 (3), 419-420.
Pérez-Barros, P., D’Amato, M.E., Guzmán, N.V., Lovrich, G.A., 2008. Taxonomic status of two South American sympatric squat lobsters, Munida gregaria and Munida subrugosa (Crustacea: Decapoda: Galatheidae), challenged by DNA sequence information. Biological Journal of the Linnean Society, 94 (2), 421-434.
Petinsaari, M., Ratnasingham, S., Miller, S.E., Hebert, P.D.N., 2020. BOLD and GenBank revisited – Do identification errors arise in the lab or in the sequence libraries? PLOS ONE, 15 (4), e0231814.
Poggiani, L., 2018. I crostacei del mare di Gano e del bacino del Metauro. Fondazione Cassa di Risparmio di Fano, Fano, 287 pp.
Poore, G.C.B., Wilson, G.D.F., 1993. Marine species richness. Nature, 361 (6413), 597-598.
Puillandre, N., Lambert, A., Brouillet, S., Achaz, G., 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21 (8), 1864- 1877. QGIS Development Team, 2009. QGIS Geographic Information System. Open Source Geospatial Foundation.
R Core Team, 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Rambaut, A., Drummond, A.J., 2012. FigTree version 1.4.0.
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.
Ratnasingham, S., Hebert, P.D.N., 2007. The Barcode of Life Data System. Molecular Ecology Notes, 77 (3), 355-364.
Raupach, M.J., Barco, A., Steinke, D., Beermann, J., Laakmann, S., 2015. The application of DNA barcodes for the identification of marine crustaceans from the North Sea and adjacent regions. PLoS ONE, 10 (9), 1-23.
Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572-1574.
Rubinoff, D., 2006. Utility of mitochondrial DNA barcodes in species conservation. Conservation Biology, 20 (4), 1026- 1033.
Rueden, C.T., Schindelin, J., Hiner, M.C., DeZonia, B.E., Walter, A. E. et al., 2017. ImageJ2: ImageJ for the next generation of scientific image data. BMC bioinformatics, 18 (1), 529.
Schlick-Steiner, B.C., Steiner, F.A., Seifert, B., Stauffer, C., Christian, E. et al., 2010. Integrative taxonomy: a multisource approach to exploring biodiversity. Annual review of entomology, 55, 421-438.
Schliep, K.P., 2011. phangorn: Phylogenetic analysis in R. Bioinformatics, 27 (4), 592-593.
Schliep, K., Potts, A.J., Morrison, D.A., Grimm, G.W., 2017. Intertwining phylogenetic trees and networks. Methods in Ecology and Evolution, 8 (10), 1212-1220.
Scorrano, S., Aglieri, G., Boero, F., Dawson, M.N., Piraino, S., 2016. Unmasking Aurelia species in the Mediterranean Sea: an integrative morphometric and molecular approach. Zoological Journal of the Linnean Society, 180 (2), 243-267.
Silva, J.M., Creer, S., dos Santos, A., Costa, A.C., Cunha, M.R. et al., 2011. Systematic and evolutionary insights derived from mtDNA COI Barcode diversity in the Decapoda (crustacea: Malacostraca). PLoS ONE, 6 (5), e19449.
Tarrío, R., Rodrıguez-Trelles, F., Ayala, F. J., 2000. Tree rooting with outgroups when they differ in their nucleotide composition from the ingroup: the drosophila saltans and willistoni groups, a case study. Molecular Phylogenetics and Evolution, 16 (3), 344-349.
Tautz, D., Arctander, P., Minelli, A., Thomas, R.H., Vogler, A. P., 2003. A plea for DNA taxonomy. Trends in Ecology and Evolution, 18 (2), 70-74.
Thallwitz, J., 1891. Decapoden-Studien, insbesondere basirt auf A.B. Meyer’s Sammlungen im Ostindischen Archipel, nebst einer Aufzählung der Decapoden und Stomatopoden des Dresdener Museums. Abhandlungen und Berichte des Königlichen Zoologischen und Anthropologisch-Etnographischen Museums zu Dresden, 3 (3), 1-56. The GIMP Development Team, June 2019. GIMP. Version 2.10.12. https: //www.gimp.org (Accessed February 2021).
Troudet, J., Grandcolas, P., Blin, A., Vignes-Lebbe, R., Legendre, F., 2017. Taxonomic bias in biodiversity data and societal preferences. Scientific Reports, 7 (1), 1-14.
Valentini, A., Pompanon, F., Taberlet, P., 2009. DNA barcoding for ecologists. Trends in Ecology and Evolution, 24 (2), 110-117. Vaquer-Sunyer, R., Duarte, C.M., 2008. Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences of the United States of America, 105 (40), 15452-15457.
Vassily, S., Simakova, U., Griffiths, H., 2017. When rare things are relatively common: caridean shrimps of the South Orkney area and distinct characteristics of the Antarctic species of Eualus (Crustacea: Decapoda: Caridea). p. 91. In: Book of abstracts: XIIth SCAR Biology Symposium. Leuven, Belgium, 10-14 July 2017. Anton Van de Putte (Ed.). Scientific Committee on Antarctic Research (SCAR), Cambridge, United Kingdom.
Wiemers, M., Fiedler, K., 2007. Does the DNA barcoding gap exist? - A case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology, 4 (8), 1-16.
Wilson, S.K., Fisher, R., Pratchett, M.S., Graham, N.A.J., Dulvy, N.K. et al., 2008. Exploitation and habitat degradation as agents of change within coral reef fish communities. Global Change Biology, 14 (12), 2796-2809.
Windig, J.J., de Kovel, C.G.F., Jong, G., 2004. Genetics and mechanics of plasticity. p. 31-49. In: Phenotypic Plasticity - Functional and Conceptual Approaches. DeWitt, T. J., Scheiner, S. M. (Eds). Oxford University Press, New York.
WoRMS Editorial Board, 2021. World Register of Marine Species (WoRMS). https://www.marinespecies.org (Accessed April 2021)
Yeates, D.K., Seago, A., Nelson, L., Cameron, S.L., Joseph, L. et al., 2011. Integrative taxonomy, or iterative taxonomy? Systematic entomology, 36 (2), 209-217.
Zariquiey Álvarez, R., 1968. Crustáceos Decápodos Ibéricos. Investigación Pesquera, 32, 1-510.
Zhang, A.B., He, L.J., Crozier, R.H., Muster, C., Zhu, C-D., 2010. Estimating sample sizes for DNA barcoding. Molecular Phylogenetics and Evolution, 54 (3), 1035-1039.