Colouration, chaetotaxy and molecular data provide species-level resolution in a species complex of Dicranocentrus (Collembola : Entomobryidae)
Feng Zhang
A E , Daoyuan Yu B C , Mark I. Stevens D and Yinhuan Ding A
+ Author Affiliations
- Author Affiliations
A Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, P. R. China.
B Soil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P. R. China.
C Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilisation, Nanjing 210014, P. R. China.
D South Australian Museum, Adelaide, SA 5000, Australia; and School of Pharmacy and Medical Sciences, University of South Australia, SA 5000, Adelaide, Australia.
E Corresponding author. Email: xtmtd.zf@gmail.com and fzhang@njau.edu.cn
Invertebrate Systematics 32(6) 1298-1315 https://doi.org/10.1071/IS18019
Submitted: 6 March 2018 Accepted: 18 June 2018 Published: 29 November 2018
Abstract
Integrative taxonomic approaches are increasingly providing species-level resolution to ‘cryptic’ diversity. In the absence of an integrative taxonomic approach, formal species validation is often lacking because of inadequate morphological diagnoses. Colouration and chaetotaxy are the most commonly used characters in collembolan taxonomy but can cause confusion in species diagnoses because these characters often have large intraspecific variation. Here, we take an integrative approach to the genus Dicranocentrus in China where four species have been previously recognised, but several members of the genus have been morphologically grouped as a species complex based on having paired outer teeth on unguis and seven colour patterns. Molecular delimitations based on distance- and evolutionary models recovered four candidate lineages from three gene markers and revealed that speciation events likely occurred during the late Neogene (4–13 million years ago). Comparison of intact dorsal chaetotaxy, whose homologies were erected on the basis of first instar larva, further validated these candidates as formal species: D. gaoligongensis, sp. nov., D. similis, sp. nov., D. pallidus, sp. nov. and D. varicolor, sp. nov., and increase the number of Dicranocentrus species from China to eight. Our study further highlights the importance of adequate taxonomy in linking morphological and molecular characters within integrative taxonomy.
Additional keywords: chaetotaxic homology, colour pattern, first instar, species delimitation.
References
Carstens, B. C., Pelletier, T. A., Reid, N. M., and Salter, J. D. (2013). How to fail at species delimitation. Molecular Ecology 22, 4369–4383.| How to fail at species delimitation.Crossref | GoogleScholarGoogle Scholar |
Christiansen, K. (1958). The Nearctic members of the genus Entomobrya (Collembola). Bulletin of the Museum of Comparative Zoology 118, 439–594.
Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
| Towards integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology 56, 879–886.
| Species concepts and species delimitation.Crossref | GoogleScholarGoogle Scholar |
Deharveng, L. (2004). Recent advances in Collembola systematics. Pedobiologia 48, 415–433.
| Recent advances in Collembola systematics.Crossref | GoogleScholarGoogle Scholar |
Ding, Y.-H., Yu, D.-Y., Guo, W.-B., Li, J.-N., and Zhang, F. (2018). Molecular phylogeny of Entomobrya (Collembola: Entomobryidae) from China: color pattern groups and multiple origins. Insect Science , .
| Molecular phylogeny of Entomobrya (Collembola: Entomobryidae) from China: color pattern groups and multiple origins.Crossref | GoogleScholarGoogle Scholar |
Fjellberg, A. (1999). The labial palp in Collembola. Zoologischer Anzeiger 237, 309–330.
Frati, F., Fanciulli, P. P., and Dallai, R. (1994). Further acquisitions on systematic relationships within the genus Orchesella (Collembola, Entomobryidae) using allozymes. Acta Zoologica Fennica 195, 35–43.
Frati, F., Dell’Ampio, E., Casasanta, S., Carapelli, A., and Fanciulli, P. P. (2000). Large amounts of genetic divergence among Italian species of the genus Orchesella (Insecta, Collembola) and the relationships of two new species. Molecular Phylogenetics and Evolution 17, 456–461.
| Large amounts of genetic divergence among Italian species of the genus Orchesella (Insecta, Collembola) and the relationships of two new species.Crossref | GoogleScholarGoogle Scholar |
Gisin, H. (1967). Espèces nouvelles et lignées évolutives de Pseudosinella endogés (Collembola). Memórias e Estudos do Museu Zoológico da Universidade de Coimbra 301, 1–25.
Greenslade, P., Stevens, M. I., Torricelli, G., and D’Haese, C. A. (2011). An ancient Antarctic endemic genus restored: morphological and molecular support for Gomphiocephalus hodgsoni (Collembola: Hypogastruridae). Systematic Entomology 36, 223–240.
| An ancient Antarctic endemic genus restored: morphological and molecular support for Gomphiocephalus hodgsoni (Collembola: Hypogastruridae).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 |
Jordana, R., and Baquero, E. (1999). Redescription of Entomobrya schoetti (Collembola, Entomobryidae, Entomobryinae), third record to the world. Boletin de Sanidad Vegetal, Plagas 25, 99–105.
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.
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.
Karanovic, T., Djurakic, M., and Eberhard, S. M. (2016). Cryptic species or inadequate taxonomy? implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa. Systematic Biology 65, 304–327.
| Cryptic species or inadequate taxonomy? implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar |
Katz, A. D., Giordano, R., and Soto-Adames, F. N. (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 |
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
Leache, A. D., and Fujita, M. K. (2010). Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings. Biological Sciences 277, 3071–3077.
| Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus).Crossref | GoogleScholarGoogle Scholar |
Mari-Mutt, J. A. (1979). A revision of the genus Dicranocentrus Schött (Insecta: Collembola: Entomobryidae). Agricultural Experiment Station University of Puerto Rico. Bulletin 259, 1–79.
Mari-Mutt, J. A. (1981a). Redescription of Willowsia jacobsoni (Börner), an entomobryid with conspicuous sexual dimorphism (Insecta: Collembola). The Journal of Agriculture of the University of Puerto Rico 65, 361–373.
Mari-Mutt, J. A. (1981b). Two new Dicranocentrus from Nepal and a key to the Indian and Nepalese species (Collembola: Entomobryidae). The Pan-Pacific Entomologist 57, 493–499.
Mari-Mutt, J. A. (1986). Puerto Rican species of Lepidocyrtus and Pseudosinella (Collembola: Entomobryidae). Caribbean Journal of Science 22, 1–48.
Papadopoulou, A., Anastasiou, I., and Vogler, A. P. (2010). Re-visiting the insect mitochondrial molecular clock: the Mid-Aegean Trench calibration. Molecular Biology and Evolution 27, 1659–1672.
| Re-visiting the insect mitochondrial molecular clock: the Mid-Aegean Trench calibration.Crossref | GoogleScholarGoogle Scholar |
Porco, D., Bedos, A., Greenslade, P., Janion, C., Skarżyński, D., Stevens, M. I., van Vuuren, B. J., and Deharveng, L. (2012). 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., Skarżyński, D., Decaëns, T., Hebert, P. D. N., and Deharveng, L. (2014). Barcoding the Collembola of Churchill: a molecular taxonomic reassessment of species diversity in a sub-Arctic area. Molecular Ecology Resources 14, 249–261.
| Barcoding the Collembola of Churchill: a molecular taxonomic reassessment of species diversity in a sub-Arctic area.Crossref | GoogleScholarGoogle Scholar |
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 |
Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). Tracer v1.6. Available at http://tree.bio.ed.ac.uk/software/tracer/ [Verified 1 March 2018].
Ramel, G., Baquero, E., and Jordana, R. (2008). Biodiversity of the Collembola fauna of Wetland Kerkini (N. Greece), with description of the sexual dimorphism of Entomobrya atrocincta Schött 1896 (Collembola: Entomobryomorpha). Annales de la Société Entomologique de France 44, 113–128.
| Biodiversity of the Collembola fauna of Wetland Kerkini (N. Greece), with description of the sexual dimorphism of Entomobrya atrocincta Schött 1896 (Collembola: Entomobryomorpha).Crossref | GoogleScholarGoogle Scholar |
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 |
Rusek, J. (2002). Taxonomy of Collembola at the beginning of the new millennium. Pedobiologia 46, 215–224.
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 |
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 |
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.
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 |
Stevens, M. I., and D’Haese, C. A. (2017). Morphologically tortured: taxonomic placement of an Antarctic springtail (Collembola: Isotomidae) misguided by morphology and ecology. Zoologica Scripta 46, 180–187.
| Morphologically tortured: taxonomic placement of an Antarctic springtail (Collembola: Isotomidae) misguided by morphology and ecology.Crossref | GoogleScholarGoogle Scholar |
Stevens, M. I., Porco, D., D’Haese, C. A., and Deharveng, L. (2011). Comment on ‘Taxonomy and the DNA Barcoding Enterprise’ by Ebach (2011). Zootaxa 2838, 85–88.
Sun, X., Zhang, F., Ding, Y., Davies, D. 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 |
Szeptycki, A. (1969). Morpho-systematic studies on Collembola. II. Postembryonic development of the chaetotaxy in Entomobryoides myrmecophlia (Reuter, 1886) (Entomobryidae). Acta Zoologica Cracoviensia 8, 163–172.
Szeptycki, A. (1979). ‘Chaetotaxy of the Entomobryidae and its Phylogenetical Significance. Morpho-systematic Studies on Collembola. IV.’ (Polska Akademia Nauk, Zakład Zoologii Systematycznej i Doświadczalnej, Państwowe Wydawnictwo Naukowe, Warszawa: Kraków, Poland.)
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 |
Thibaud, J.-M. (1967). Contribution à l’étude du développement postembryonnaire chez les Collemboles Hypogastruridae épigés et cavernicoles (1re note). Annales de Spéléologie 22, 167–198.
Will, K. P., Mishler, B. D., and Wheeler, Q. D. (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology 54, 844–851.
| The perils of DNA barcoding and the need for integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
Xisto, T., and Mendonça, M. C. (2016). Two new species of Dicranocentrus Schött, 1893 (Collembola: Entomobryidae) from Serra do Gandarela, Minas Gerais State, Brazil. Zootaxa 4079, 217–228.
| Two new species of Dicranocentrus Schött, 1893 (Collembola: Entomobryidae) from Serra do Gandarela, Minas Gerais State, Brazil.Crossref | GoogleScholarGoogle Scholar |
Xisto, T., and Mendonça, M. C. (2018). New species and new records of Dicranocentrus Schött, 1893 (Collembola: Entomobryidae) from southeastern Brazil. Insect Systematics & Evolution 49, 23–58.
| New species and new records of Dicranocentrus Schött, 1893 (Collembola: Entomobryidae) from southeastern Brazil.Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
Yu, D., Qin, C., Ding, Y., Hu, F., Zhang, F., and Liu, M. (2018). Revealing species diversity of Tomocerus ocreatus complex (Collembola: Tomoceridae): integrative species delimitation and evaluation of taxonomic characters. Arthropod Systematics & Phylogeny 76, 147–172.
Zhang, F., and Deharveng, L. (2015). Systematic revision of Entomobryidae (Collembola) by integrating molecular and new morphological evidence. Zoologica Scripta 44, 298–311.
| Systematic revision of Entomobryidae (Collembola) by integrating molecular and new morphological evidence.Crossref | GoogleScholarGoogle Scholar |
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 |
Zhang, F., Yu, D., Luo, Y., Ho, S. Y. W., Wang, B., and Zhu, C. (2014). Cryptic diversity, diversification and vicariance in the two species complexes of Tomocerus (Collembola, Tomoceridae) from China. Zoologica Scripta 43, 393–404.
| Cryptic diversity, diversification and vicariance in the two species complexes of Tomocerus (Collembola, Tomoceridae) from China.Crossref | GoogleScholarGoogle Scholar |
Zhang, F., Bedos, A., and Deharveng, L. (2016). Cave-dwelling Coecobrya from southern China with a survey of clypeal chaetae in Entomobryoidea (Collembola). European Journal of Taxonomy 226, 1–21.
Zhang, F., Jantarit, S., Nilsai, A., Stevens, M. I., Ding, Y., and Satasook, C. (2018). 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 |
