Untangling Lepidocyrtus (Collembola, Entomobryidae): new molecular data shed light on the relationships of the European groups
Eduardo Mateos A D , Paula Escuer B , Galina Buşmachiu C , Marta Riutort B and Marta Álvarez-Presas B
+ Author Affiliations
- Author Affiliations
A Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal, 643, 08028 Barcelona, Spain.
B Departament de Genètica, Microbiologia i Estadistica, Facultat de Biologia, Universitat de Barcelona, Spain.
C Institute of Zoology, Academy of Sciences of Moldova, 2028 Chişinău, Republic of Moldova.
D Corresponding author. Email: emateos@ub.edu
Invertebrate Systematics 32(3) 639-651 https://doi.org/10.1071/IS17056
Submitted: 22 June 2017 Accepted: 5 October 2017 Published: 8 May 2018
Abstract
European Lepidocyrtus species are usually grouped into five species-groups within two subgenera, Lepidocyrtus s.s. and Lanocyrtus, defined by the distribution of scale covering and dorsal head and body macrochaetotaxy. The discovery of several Lepidocyrtus populations with morphological characters intermediate between two species-groups suggested the need for the present study to test whether molecular data provide support to these groups. The morphology and gene sequences of 110 specimens belonging to 19 species of European Lepidocyrtus have been studied. Our molecular results are congruent with the distribution of the European species into the five groups established in the literature on the basis of morphological characters, but also indicated that subgenus Lanocyrtus is paraphyletic while subgenus Lepidocyrtus s.s. is monophyletic. A new species, Lepidocyrtus intermedius, is described, and a redefinition of European species-groups is proposed based on chaetotaxy.
Additional keywords: chaetotaxy, COXII, EF-1α, cryptic species, DNA, evolution, phylogeny, taxonomy.
References
Akaike, H. (1973). Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika 60, 255–265.| Maximum likelihood identification of Gaussian autoregressive moving average models.Crossref | GoogleScholarGoogle Scholar |
Bellinger, P. F., Christiansen, K. A., and Janssens, F. (1996–2017). Checklist of the Collembola of the World. Available at: http://www.collembola.org [Accessed 31 May 2017].
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=1b4ae107a4d41c6cf044947b82a73459CAS |
Christiansen, K. A., and Bellinger, P. F. (1980). ‘The Collembola of North America North of Rio Grande, a Taxonomic Analysis.’ (Grinnell College: Grinnell, IA.)
Cicconardi, F., Nardi, F., Emerson, B. C., Frati, F., and Fanciulli, P. P. (2010). Deep phylogeographic divisions and long-term persistence of forest invertebrates (Hexapoda: Collembola) in the north-western Mediterranean basin. Molecular Ecology 19, 386–400.
| Deep phylogeographic divisions and long-term persistence of forest invertebrates (Hexapoda: Collembola) in the north-western Mediterranean basin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOntLc%3D&md5=d13549612b8562e1c3c39d3e7863d8afCAS |
Cicconardi, F., Fanciulli, P. P., and Emerson, B. C. (2013). Collembola, the biological species concept and the underestimation of global species richness. Molecular Ecology 22, 5382–5396.
| Collembola, the biological species concept and the underestimation of global species richness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Ors7vE&md5=9a42f5eb8cf9e1827c0f3c79135d7422CAS |
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=8455a3ff18c54ee00d48a1421d4dba7aCAS |
Delamare-Deboutteville, C. (1948). Recherches sur les Collemboles termitophiles et myrmécophiles (Ecologie, Ethologie, Systématique). Archives de Zoologie Expérimentale et Générale 85, 261–425.
Fabricius, J. C. (1793). ‘Entomologia Systematica Emendata et Aucta, Secundum Classes, ordines, genera, species adjectis synonimis, locis, observationibus, descriptionibus. Volume 2.’ (C. G. Proft: Hafniae.)
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 |
Fjellberg, A. (1999). The labial palp in Collembola. Zoologischer Anzeiger 237, 309–330.
Fjellberg, A. (2007). The Collembola of Fennoscandia and Denmark. Part II: Entomobryomorpha and Symphypleona. In ‘Fauna Entomologica Scandinavica. Volume 42’. (Eds. Kristensen, N.P. and Michelsen, V.). pp 1–264. (Brill: Leiden, The Netherlands)
Gisin, H. (1963). Collemboles d’Europe V. Revue Suisse de Zoologie 7, 77–101.
Gisin, H. (1964a). Collemboles d’Europe VI. Revue Suisse de Zoologie 71, 383–400.
| Collemboles d’Europe VI.Crossref | GoogleScholarGoogle Scholar |
Gisin, H. (1964b). Collemboles d’Europe VII. Revue Suisse de Zoologie 71, 649–678.
Gisin, H. (1965). Nouvelles notes taxonomiques sur les Lepidocyrtus. Revue d’Écologie et de Biologie du Sol 2, 519–524.
Gisin, H. (1967). Espèces nouvelles et lignées évolutives de Pseudosinella endogés (Collembola). Memórias e Estudos do Museu Zoológico da Universidade de Coimbra 301, 6–25.
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.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=51032c35c9b55c2e0a0ae6daa653f17bCAS |
Huelsenbeck, J. P., and Ronquist, F. (2005). Bayesian analysis of molecular evolution using MrBayes. In ‘Statistical Methods in Molecular Evolution’ (Ed. Nielsen, R.), pp. 183–226. (Springer: New York, NY.)
Hüther, W. (1971). Collembolen von einem Hamburger Müllplatz. Entomologische Mitteilungen aus dem Zoologischen Museum Hamburg 72, 157–165.
Hüther, W. (1986). New aspects in taxonomy of Lepidocyrtus (Collembola). In ‘2nd International Seminar on Apterygota’. (Ed. R. Dallai.) pp. 61–65. (University of Siena, Siena, Italy)
Jordana, R., and Baquero, E. (2005). A proposal of characters for taxonomic identification of Entomobrya species (Collembola, Entomobryomorpha), with description of a new species. Abhandlungen und Berichte des Naturkundemuseums Görlitz 76, 117–134.
Katz, A. D., Giordano, R., and Soto-Adames, F. N. (2015). Operational criteria for cryptic species delimitation when evidence is limited, as exemplified by North American Entomobrya (Collembola: Entomobryidae). Zoological Journal of the Linnean Society 173, 818–840.
| Operational criteria for cryptic species delimitation when evidence is limited, as exemplified by North American Entomobrya (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33, 1870–1874.
| 1:CAS:528:DC%2BC28XhsF2ltrzN&md5=bcbd369c661cdc481de05ecb4f74d120CAS |
Larkin, M. A., and Blackshields, G. (2007). ClustalW and ClustalX version 2. Bioinformatics 23, 2947–2948.
| ClustalW and ClustalX version 2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=14e869137f5d6f9ed274ee8f26511ddbCAS |
Letunic, I., and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128.
| Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlGktLzN&md5=79f38ab21d10b509875cad0762cac144CAS |
Mari Mutt, J. A. (1979). A revision of the genus Dicranocentrus Schött (Insecta: Collembola: Entomobryidae). Agricultural Experiment Station University of Puerto Rico 259, 1–79.
Mari Mutt, J. A. (1986). Puerto Rican species of Lepidocyrtus and Pseudosinella (Collembola: Entomobryidae). Caribbean Journal of Science 22, 1–48.
Mateos, E. (2008a). The European Lepidocyrtus Bourlet, 1839 (Collembola: Entomobryidae). Zootaxa 1769, 35–59.
Mateos, E. (2008b). Definition of Lepidocyrtus lusitanicus Gama, 1964 species-complex (Collembola, Entomobryidae), with description of new species and color forms from the Iberian Peninsula. Zootaxa 1917, 38–54.
Mateos, E. (2011). New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae). Zootaxa 3108, 25–40.
Mateos, E. (2012). The European Lepidocyrtus lanuginosus group (Collembola: Entomobryidae), definition and description of a new species from Spain. Zootaxa 3570, 69–81.
Mateos, E., and Greenslade, P. (2015). Towards understanding Lepidocyrtus Bourlet, 1839 (Collembola, Entomobryidae) I: diagnosis of the subgenus Setogaster, new records and redescriptions of species. Zootaxa 4044, 105–129.
| Towards understanding Lepidocyrtus Bourlet, 1839 (Collembola, Entomobryidae) I: diagnosis of the subgenus Setogaster, new records and redescriptions of species.Crossref | GoogleScholarGoogle Scholar |
Mateos, E., and Petersen, H. (2012). Definition of the European Lepidocyrtus curvicollis group (Collembola: Entomobryidae) with description of a new species from Sardinia (Italy). Zootaxa 3273, 51–62.
Rambaut, A. (2009). ‘FigTree, a Graphical Viewer of Phylogenetic Trees.’ (Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, United Kingdom)
Snider, R. J. (1967). The chaetotaxy of North American Lepidocyrtus s. str., (Collembola: Entomobryidae). Contributions of the American Entomological Institute 2, 1–28.
Soto-Adames, F. N. (2000). Phylogeny of Neotropical Lepidocyrtus (Collembola: Entomobryidae): first assessment of patterns of speciation in Puerto Rico and phylogenetic relevance of some subgeneric diagnostic characters. Systematic Entomology 25, 485–502.
| Phylogeny of Neotropical Lepidocyrtus (Collembola: Entomobryidae): first assessment of patterns of speciation in Puerto Rico and phylogenetic relevance of some subgeneric diagnostic characters.Crossref | GoogleScholarGoogle Scholar |
Soto-Adames, F. N. (2002). Molecular phylogeny of the Puerto Rican Lepidocyrtus and Pseudosinella (Hexapoda: Collembola), a validation of Yoshii’s ‘colour pattern species’. Molecular Phylogenetics and Evolution 25, 27–42.
| Molecular phylogeny of the Puerto Rican Lepidocyrtus and Pseudosinella (Hexapoda: Collembola), a validation of Yoshii’s ‘colour pattern species’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVeqs74%3D&md5=ce2b1dac8dfa3411482b8ab2facdc113CAS |
Soto-Adames, F. N. (2008). Postembryonic development of the dorsal chaetotaxy in Seira dowlingi (Collembola, Entomobryidae); with an analysis of the diagnostic and phylogenetic significance of primary chaetotaxy in Seira. Zootaxa 1683, 1–31.
Soto-Adames, F. N. (2010). Two new species and descriptive notes for five Pseudosinella species (Hexapoda: Collembola: Entomobryidae) from West Virginian (USA) caves. Zootaxa 2331, 1–34.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=bf1c47d07b064fc1a91a82830ae5d513CAS |
Szeptycki, A. (1972). Morpho-systematic studies on Collembola III. Body chaetotaxy in the first instars of several genera of the Entomobryomorpha. Acta Zoologica Cracoviensia 17, 341–372.
Szeptycki, A. (1973). North Korean Collembola. I. The genus Homidia Börner, 1906 (Entomobryidae). Acta Zoological Cracoviensia 18, 23–39.
Szeptycki, A. (1979). ‘Chaetotaxy of the Entomobryidae and its Phylogenetical Significance. Morpho-systematic Studies of Collembola, IV.’ (Polska Akademia Nauk, Zakład Zoologii Systematycznej i Doświadczalnej: Kraków, Poland.)
Wang, F., Chen, J. X., and Christiansen, K. (2003). Taxonomy of the genus Lepidocyrtus s.l. (Collembola: Entomobryidae) in East and Southeast Asia and Malaysia, with description of a new species from the People’s Republic of China. Canadian Entomologist 135, 823–837.
| Taxonomy of the genus Lepidocyrtus s.l. (Collembola: Entomobryidae) in East and Southeast Asia and Malaysia, with description of a new species from the People’s Republic of China.Crossref | GoogleScholarGoogle Scholar |
Winkler, D. (2017). New Lepidocyrtus Bourlet, 1839 from riverine woodland in Hungary (Collembola, Entomobryidae). Zootaxa 4250, 529–540.
| New Lepidocyrtus Bourlet, 1839 from riverine woodland in Hungary (Collembola, Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Winkler, D., and Traser, G. (2012). Explanation of the European Lepidocyrtus pallidus–serbicus group (Collembola, Entomobryidae), with description of new species from Hungary. Zootaxa 3394, 35–47.
Yu, D., Zhang, F., Stevens, M. I., Yan, Q., Liu, M., and Hu, F. (2016). New insight into the systematics of Tomoceridae (Hexapoda, Collembola) by integrating molecular and morphological evidence. Zoologica Scripta 45, 286–299.
| New insight into the systematics of Tomoceridae (Hexapoda, Collembola) by integrating molecular and morphological evidence.Crossref | GoogleScholarGoogle Scholar |
Zhang, F., and Deharveng, L. (2014). Systematic revision of Entomobryidae (Collembola) by integrating molecular and new morphological evidence. Zoologica Scripta 44, 298–311.
Zhang, F., Sun, D. D., Yu, D. Y., and Wang, B. X. (2015). Molecular phylogeny supports S-chaetae as a key character better than jumping organs and body scales in classification of Entomobryoidea (Collembola). Scientific Reports 5, 1–12.
