DNA-based approaches uncover cryptic diversity in the European Lepidocyrtus lanuginosus species group (Collembola: Entomobryidae)
Bing Zhang
A E , Ting-Wen Chen A B , Eduardo Mateos C , Stefan Scheu A D and Ina Schaefer A
+ Author Affiliations
- Author Affiliations
A J. F. Blumenbach Institute of Zoology and Anthropology, Animal Ecology, University of Göttingen, Untere Karspüle 2, 37073 Göttingen, Germany.
B Institute of Soil Biology, Biology Centre, Czech Academy of Sciences, Na Sádkách 7, 37005 České Budějovice, Czech Republic.
C Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 643, 08028 Barcelona, Spain.
D Centre of Biodiversity and Sustainable Land Use, University of Göttingen, Von-Siebold-Str. 8, 37075 Göttingen, Germany.
E Corresponding author. Email: bzhang3@gwdg.de
Invertebrate Systematics 33(4) 661-670 https://doi.org/10.1071/IS18068
Submitted: 10 August 2018 Accepted: 27 March 2019 Published: 6 August 2019
Abstract
DNA sequence data and phylogenies are useful tools for species delimitation, especially in taxa comprising cryptic species. The Lepidocyrtus lanuginosus species group (Collembola: Entomobryidae) comprises three morphospecies and distinct cryptic species. We applied three DNA-based methods to delimit species boundaries in the L. lanuginosus species group across central and southern Europe. Using cytochrome c oxidase subunit I and II, we identified gaps of genetic distances that indicate species boundaries and found 10 and 9 distinct genetic lineages in L. cyaneus and L. lanuginosus, respectively. The nuclear gene elongation factor 1-α delimited 89% of the lineages but 28S rDNA (D1–2 domain) was too conserved for this purpose. The phylogenetic trees showed that L. cyaneus and L. lanuginosus are polyphyletic, suggesting that body colour is insufficient for delimiting species in the L. lanuginosus species group. Our study challenges the current morphology-based species delimitation in the L. lanuginosus species group and suggests that molecular approaches are needed for fast and accurate determination of Collembola species in both taxonomic and ecological studies. Overall, the results suggest that wide geographic sampling combined with molecular phylogenetic approaches is needed to delimit species and to understand the full range of cryptic diversity in Collembola.
Additional keywords: barcoding, colour, cytochrome c oxidase subunit I and II, elongation factor 1-α, ribosomal subunit 28S rDNA D1–2 domain, springtail.
References
Anslan, S., and Tedersoo, L. (2015). Performance of cytochrome c oxidase subunit I (COI), ribosomal DNA Large Subunit (LSU) and Internal Transcribed Spacer 2 (ITS2) in DNA barcoding of Collembola. European Journal of Soil Biology 69, 1–7.| Performance of cytochrome c oxidase subunit I (COI), ribosomal DNA Large Subunit (LSU) and Internal Transcribed Spacer 2 (ITS2) in DNA barcoding of Collembola.Crossref | GoogleScholarGoogle Scholar |
Bellinger, P. F., Christiansen, K. A., and Janssens, F. (1996). Checklist of the Collembola of the World. Available at: http://www.collembola.org/ [accessed 26 June 2018].
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K., and Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
| Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |
Carstens, B. C., Pelletier, T. A., Reid, N. M., and Satler, J. D. (2013). How to fail at species delimitation. Molecular Ecology 22, 4369–4383.
| How to fail at species delimitation.Crossref | GoogleScholarGoogle Scholar | 23855767PubMed |
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 | 20015142PubMed |
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 | 24112308PubMed |
D’Haese, C. A. (2002). Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment. Proceedings of the Royal Society B: Biological Sciences 269, 1143–1151.
| Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment.Crossref | GoogleScholarGoogle Scholar | 12061958PubMed |
De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology 56, 879–886.
| Species concepts and species delimitation.Crossref | GoogleScholarGoogle Scholar | 18027281PubMed |
Ding, Y., Yu, D., Guo, W., Li, J., and Zhang, F. (2018). Molecular phylogeny of Entomobrya (Collembola: Entomobryidae) from China: color pattern groups and multiple origins. Insect Science 26, 587–597.
| Molecular phylogeny of Entomobrya (Collembola: Entomobryidae) from China: color pattern groups and multiple origins.Crossref | GoogleScholarGoogle Scholar | 29135078PubMed |
Felderhoff, K. L., Bernard, E. C., and Moulton, J. K. (2010). Survey of Pogonognathellus Börner (Collembola: Tomoceridae) in the southern Appalachians based on morphological and molecular data. Annals of the Entomological Society of America 103, 472–491.
| Survey of Pogonognathellus Börner (Collembola: Tomoceridae) in the southern Appalachians based on morphological and molecular data.Crossref | GoogleScholarGoogle Scholar |
Feulner, P. G. D., Kirschbaum, F., Schugardt, C., Ketmaier, V., and Tiedemann, R. (2006). Electrophysiological and molecular genetic evidence for sympatrically occuring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus). Molecular Phylogenetics and Evolution 39, 198–208.
| Electrophysiological and molecular genetic evidence for sympatrically occuring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus).Crossref | GoogleScholarGoogle Scholar |
Fjellberg, A. (2007). ‘The Collembola of Fennoscandia and Denmark. Part II: Entomobryomorpha and Symphypleona.’ (Ed. N. P. Kristensen.) (Brill: Boston.)
Grundt, H. H., Kjolner, S., Borgen, L., Rieseberg, L. H., and Brochmann, C. (2006). High biological species diversity in the arctic flora. Proceedings of the National Academy of Sciences of the United States of America 103, 972–975.
| High biological species diversity in the arctic flora.Crossref | GoogleScholarGoogle Scholar | 16418291PubMed |
Hailer, F., Kutschera, V. E., Hallström, B. M., Klassert, D., Fain, S. R., Leonard, J. A., Arnason, U., and Janke, A. (2012). Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage. Science 336, 344–347.
| Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage.Crossref | GoogleScholarGoogle Scholar | 22517859PubMed |
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. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.
| Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar |
Heled, J., and Drummond, A. J. (2010). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570–580.
| Bayesian inference of species trees from multilocus data.Crossref | GoogleScholarGoogle Scholar | 19906793PubMed |
Hopkin, S. P. (Ed.) (1997). ‘Biology of the Springtails (Insecta: Collembola).’ (Oxford University Press: Oxford.)
Hopkin, S. P. (Ed.) (2007). ‘A Key to the Springtails (Collembola) of Britain and Ireland’. (FSC Publicatio: Shrewsbury, UK.)
Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A., and Flouri, T. (2017). Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630–1638.
| Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo.Crossref | GoogleScholarGoogle Scholar | 28108445PubMed |
Katz, A. D., Giordano, R., and Soto-Adames, F. (2015a). Taxonomic review and phylogenetic analysis of fifteen North American Entomobrya (Collembola, Entomobryidae), including four new species. ZooKeys 525, 1–75.
| Taxonomic review and phylogenetic analysis of fifteen North American Entomobrya (Collembola, Entomobryidae), including four new species.Crossref | GoogleScholarGoogle Scholar |
Katz, A. D., Giordano, R., and Soto-Adames, F. N. (2015b). 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 |
Kempson, D., Lloyd, M., and Ghelardi, R. (1963). A new extractor for woodland litter. Pedobiologia 3, 1–30.
Knowles, L. L., and Carstens, B. C. (2007). Delimiting species without monophyletic gene trees. Systematic Biology 56, 887–895.
| Delimiting species without monophyletic gene trees.Crossref | GoogleScholarGoogle Scholar | 18027282PubMed |
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.
| Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 28013191PubMed |
Leaché, A. D., and Fujita, M. K. (2010). Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B: Biological Sciences 277, 3071–3077.
| Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus).Crossref | GoogleScholarGoogle Scholar | 20519219PubMed |
Mateos, E. (2008a). 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.
| Definition of Lepidocyrtus lusitanicus Gama, 1964 species-complex (Collembola, Entomobryidae), with description of new species and color forms from the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |
Mateos, E. (2008b). The European Lepidocyrtus Bourlet, 1839 (Collembola: Entomobryidae). Zootaxa 1769, 35–59.
Mateos, E. (2011). New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae). Zootaxa 3108, 25–40.
| New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
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 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.
| Definition of the European Lepidocyrtus curvicollis group (Collembola: Entomobryidae) with description of a new species from Sardinia (Italy).Crossref | GoogleScholarGoogle Scholar |
Mateos, E., Escuer, P., Buşmachiu, G., Riutort, M., and Álvarez-Presas, M. (2018). Untangling Lepidocyrtus (Collembola, Entomobryidae): new molecular data shed light on the relationships of the European groups. Invertebrate Systematics 32, 639–651.
| Untangling Lepidocyrtus (Collembola, Entomobryidae): new molecular data shed light on the relationships of the European groups.Crossref | GoogleScholarGoogle Scholar |
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘2010 Gateway Computing Environments Workshop (GCE)’. pp. 1–8. (IEEE: New Orleans, LA.)
Nilsai, A., Jantarit, S., Satasook, C., and Zhang, F. (2017). Three new species of Coecobrya (Collembola: Entomobryidae) from caves in the Thai peninsula. Zootaxa 4286, 187–202.
| Three new species of Coecobrya (Collembola: Entomobryidae) from caves in the Thai peninsula.Crossref | GoogleScholarGoogle Scholar |
Porco, D., Bedos, A., Greenslade, P., Janion, C., Skarzyński, D., Stevens, M. I., Jansen Van Vuuren, B., and Deharveng, L. (2012a). Challenging species delimitation in Collembola: cryptic diversity among common springtails unveiled by DNA barcoding. Invertebrate Systematics 26, 470–477.
| Challenging species delimitation in Collembola: cryptic diversity among common springtails unveiled by DNA barcoding.Crossref | GoogleScholarGoogle Scholar |
Porco, D., Potapov, M., Bedos, A., Busmachiu, G., Weiner, W. M., Hamra-Kroua, S., and Deharveng, L. (2012b). Cryptic diversity in the ubiquist species Parisotoma notabilis (Collembola, Isotomidae): a long-used chimeric species? PLoS One 7, e46056.
| Cryptic diversity in the ubiquist species Parisotoma notabilis (Collembola, Isotomidae): a long-used chimeric species?Crossref | GoogleScholarGoogle Scholar | 23049931PubMed |
Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
| ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |
Rambaut, A., Drummond, A. J., and Suchard, M. A. (2013). Tracer v1.6. Available from: http://beast.bio.ed.ac.uk/Tracer [accessed 26 June 2018].
Rannala, B., and Yang, Z. (2003). Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164, 1645–1656.
| 12930768PubMed |
Rannala, B., and Yang, Z. (2013). Improved reversible jump algorithms for Bayesian species delimitation. Genetics 194, 245–253.
| Improved reversible jump algorithms for Bayesian species delimitation.Crossref | GoogleScholarGoogle Scholar | 23502678PubMed |
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Rougerie, R., Decaëns, T., Deharveng, L., Porco, D., James, S. W., Chang, C. H., Richard, B., Potapov, M., Suhardjono, Y., and Hebert, P. D. N. (2009). DNA barcodes for soil animal taxonomy. Pesquisa Agropecuária Brasileira 44, 789–802.
| DNA barcodes for soil animal taxonomy.Crossref | GoogleScholarGoogle Scholar |
Rusek, J. (2002). Taxonomy of Collembola at the beginning of the new millennium. Pedobiologia 46, 215–224.
| Taxonomy of Collembola at the beginning of the new millennium.Crossref | GoogleScholarGoogle Scholar |
Salmon, S., Ponge, J. F., Gachet, S., Deharveng, L., Lefebvre, N., and Delabrosse, F. (2014). Linking species, traits and habitat characteristics of Collembola at European scale. Soil Biology & Biochemistry 75, 73–85.
| Linking species, traits and habitat characteristics of Collembola at European scale.Crossref | GoogleScholarGoogle Scholar |
Samadi, S., and Barberousse, A. (2006). The tree, the network, and the species. Biological Journal of the Linnean Society. Linnean Society of London 89, 509–521.
| The tree, the network, and the species.Crossref | GoogleScholarGoogle Scholar |
Schneider, C., and D’Haese, C. A. (2013). Morphological and molecular insights on Megalothorax: the largest Neelipleona genus revisited (Collembola). Invertebrate Systematics 27, 317–364.
| Morphological and molecular insights on Megalothorax: the largest Neelipleona genus revisited (Collembola).Crossref | GoogleScholarGoogle Scholar |
Sonnenberg, R., Nolte, A. W., and Tautz, D. (2007). An evaluation of LSU rDNA D1–D2 sequences for their use in species identification. Frontiers in Zoology 4, 6.
| An evaluation of LSU rDNA D1–D2 sequences for their use in species identification.Crossref | GoogleScholarGoogle Scholar | 17306026PubMed |
Soto-Adames, F. N. (2002). Molecular phylogeny of the Puerto Rican Lepidocyrtus and Pseudosinella (Hexapoda: Collembola), a validation of Yoshii’s “color 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 “color pattern species”.Crossref | GoogleScholarGoogle Scholar | 12383748PubMed |
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
| RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |
Struck, T. H., Feder, J. L., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V. I., Kistenich, S., Larsson, K. H., Liow, L. H., Nowak, M. D., Stedje, B., Bachmann, L., and Dimitrov, D. (2018). Finding evolutionary processes hidden in cryptic species. Trends in Ecology & Evolution 33, 153–163.
| Finding evolutionary processes hidden in cryptic species.Crossref | GoogleScholarGoogle Scholar |
Sun, X., Zhang, F., Ding, Y., Davies, T. W., Li, Y., and Wu, D. (2017). Delimiting species of Protaphorura (Collembola: Onychiuridae): integrative evidence based on morphology, DNA sequences and geography. Scientific Reports 7, 8261.
| Delimiting species of Protaphorura (Collembola: Onychiuridae): integrative evidence based on morphology, DNA sequences and geography.Crossref | GoogleScholarGoogle Scholar | 28811535PubMed |
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 21546353PubMed |
Thompson, J. D., Higgins, D. G., and 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, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |
Traser, G., and Dányi, L. (2008). Lepidocyrtus mariani sp. n., a new springtail species from Hungary (Collembola: Entomobryidae). Opuscula Entomologica 39, 91–98.
Vaidya, G., Lohman, D. J., and Meier, R. (2011). SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180.
| SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information.Crossref | GoogleScholarGoogle Scholar |
von Saltzwedel, H., Scheu, S., and Schaefer, I. (2017). Genetic structure and distribution of Parisotoma notabilis (Collembola) in Europe: cryptic diversity, split of lineages and colonization patterns. PLoS One 12, e0170909.
| Genetic structure and distribution of Parisotoma notabilis (Collembola) in Europe: cryptic diversity, split of lineages and colonization patterns.Crossref | GoogleScholarGoogle Scholar | 28170395PubMed |
Wiens, J. J. (2007). Species delimitation: new approaches for discovering diversity. Systematic Biology 56, 875–878.
| Species delimitation: new approaches for discovering diversity.Crossref | GoogleScholarGoogle Scholar | 18027280PubMed |
Winkler, D. (2016). A new species of Lepidocyrtus (Collembola, Entomobryidae) from the Börzsöny Mountains, Hungary. Zootaxa 4150, 388–400.
| A new species of Lepidocyrtus (Collembola, Entomobryidae) from the Börzsöny Mountains, Hungary.Crossref | GoogleScholarGoogle Scholar | 27615681PubMed |
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 | 28609993PubMed |
Winkler, D., and Traser, G. N. (2012). Explanation of the European Lepidocyrtus pallidus-serbicus group (Collembola, Entomobryidae), with description of new species from Hungary. Zootaxa 3394, 35–47.
Yang, Z., and 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.
| Bayesian species delimitation using multilocus sequence data.Crossref | GoogleScholarGoogle Scholar | 20439743PubMed |
Yang, Z., and Rannala, B. (2017). Bayesian species identification under the multispecies coalescent provides significant improvements to DNA barcoding analyses. Molecular Ecology 26, 3028–3036.
| Bayesian species identification under the multispecies coalescent provides significant improvements to DNA barcoding analyses.Crossref | GoogleScholarGoogle Scholar | 28281309PubMed |
Yu, D., Ding, Y., and Ma, Y. (2017). Revision of Tomocerus similis Chen & Ma, with discussion of the kinoshitai complex and the distal tibiotarsal chaetae in Tomocerinae (Collembola, Tomoceridae). Zootaxa 4268, 395–410.
| Revision of Tomocerus similis Chen & Ma, with discussion of the kinoshitai complex and the distal tibiotarsal chaetae in Tomocerinae (Collembola, Tomoceridae).Crossref | GoogleScholarGoogle Scholar | 28610364PubMed |
Zhang, C., Rannala, B., and Yang, Z. (2012). Robustness of compound dirichlet priors for Bayesian inference of branch lengths. Systematic Biology 61, 779–784.
| Robustness of compound dirichlet priors for Bayesian inference of branch lengths.Crossref | GoogleScholarGoogle Scholar | 22328570PubMed |
Zhang, J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.
| A general species delimitation method with applications to phylogenetic placements.Crossref | GoogleScholarGoogle Scholar | 23990417PubMed |
Zhang, F., Yu, D., Luo, Y., Ho, S. Y. W., Wang, B., and Zhu, C. (2014). Cryptic diversity, diversification and vicariance in two species complexes of Tomocerus (Collembola, Tomoceridae) from China. Zoologica Scripta 43, 393–404.
| Cryptic diversity, diversification and vicariance in two species complexes of Tomocerus (Collembola, Tomoceridae) from China.Crossref | GoogleScholarGoogle Scholar |
Zhang, B., Chen, T. W., Mateos, E., Scheu, S., and Schaefer, I. (2018a). Cryptic species in Lepidocyrtus lanuginosus (Collembola: Entomobryidae) are sorted by habitat type. Pedobiologia 68, 12–19.
| Cryptic species in Lepidocyrtus lanuginosus (Collembola: Entomobryidae) are sorted by habitat type.Crossref | GoogleScholarGoogle Scholar |
Zhang, F., Jantarit, S., Nilsai, A., Stevens, M. I., Ding, Y., and Satasook, C. (2018b). Species delimitation in the morphologically conserved Coecobrya (Collembola: Entomobryidae): a case study integrating morphology and molecular traits to advance current taxonomy. Zoologica Scripta 47, 342–356.
| Species delimitation in the morphologically conserved Coecobrya (Collembola: Entomobryidae): a case study integrating morphology and molecular traits to advance current taxonomy.Crossref | GoogleScholarGoogle Scholar |
