Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Morphological and molecular insights on Megalothorax: the largest Neelipleona genus revisited (Collembola)

Clément Schneider A B and Cyrille A. D’Haese A
+ Author Affiliations
- Author Affiliations

A UMR 7205 CNRS-MNHN, Dpt Systématique & Evolution, Muséum National d’Histoire Naturelle, CP50, 45 rue Buffon, 75005 Paris, France.

B Corresponding author. Email: clement.schneider@mnhn.fr

Invertebrate Systematics 27(3) 317-364 https://doi.org/10.1071/IS13002
Submitted: 12 November 2012  Accepted: 2 April 2013   Published: 25 June 2013

Abstract

The genus Megalothorax Willem, 1900 is redefined along with a redescription of the type species M. minimus Willem, 1900 and the description of five new species (M. granulosus, sp. nov., M. nigropunctatus, sp. nov., M. perspicillum, sp. nov., M. svalbardensis, sp. nov. and M. willemi, sp. nov.). We describe and comment on broad sets of discriminating characters for Megalothorax systematics. For the first time, trichobothria are recorded for Neelipleona, probably of generic importance. The described species are provided with DNA data (COI, 16S and 28S) and included in a molecular-based phylogenetic analysis. The traditional distinction between minimus-group and incertus-group is discussed in the light of DNA and morphology components. A key to the worldwide Megalothorax species is provided.

Additional keywords: chaetotaxy, DNA barcoding, key, morphology, Neelidae, neotype, new species, phylogeny, systematics, taxonomy, trichobothria.


References

Babenko, A. (2000). Collembolan assemblages of polar deserts and subarctic nival communities. Pedobiologia 44, 421–429.
Collembolan assemblages of polar deserts and subarctic nival communities.Crossref | GoogleScholarGoogle Scholar |

Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K., 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 |

Bonet, F. (1947). Monografia de la familia Neelidae (Collembola). Revista de la Sociedad Mexicana de Historia Natural 8, 131–144.

Bretfeld, G. (1999). Symphypleona. In ‘Synopses on Palaearctic Collembola. Vol. 2’. (Ed. W. Dunger.) Abhandlungen und Berichte des Naturkundemuseum Görlitz 71(1), 1–318.

Bretfeld, G., and Griegel, A. (1999). Description of a new Neelidae genus and species and of new specimens of Sminthurides annulicornis Axelson 1905 from Poland. Senckenbergiana Biologica 79, 211–223.

Chagnon, M., and Paré, D. (2000). Relationships between soil chemistry, microbial biomass and the collembolan fauna of southern Québec suger maple stands. Ecoscience 7, 307–316.

Christian, E. (1998). Megalothorax sanctistephani sp.n. (Insecta: Collembola: Neelidae) from the catacombs of St. Stephen’s Cathedral, Vienna. Annalen des Naturhistorischen Museums, Wien 100B, 15–18.

Christiansen, K., and Bellinger, P. (1992). Collembola. Insects of Hawaii 15, 1–445.

Christiansen, K., and Bellinger, P. (1998). ‘The Collembola of North America, north of the Rio Grande: a taxonomic analysis. Part 4. Families Neelidae, Sminthuridae and Mackenziellidae. Glossary. Bibliography. Index.’ pp. 1175–1520. (Grinnell College: Iowa, USA.)

Collinge, W. E., and Shoebotham, J. W. (1909). Description of a new genus of Collembola of the family Neelidae, Folsom. The Journal of Economic Biology 4, 45–50.

Culik, M. P., and Filho, D. Z. (2003). Diversity and distribution of Collembola (Arthropoda: Hexapoda) of Brazil. Biodiversity and Conservation 12, 1119–1143.
Diversity and distribution of Collembola (Arthropoda: Hexapoda) of Brazil.Crossref | GoogleScholarGoogle Scholar |

D’Haese, C. A. (2002). Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and Optimization Alignment. Proceedings. 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 | 1:CAS:528:DC%2BD38Xls1aqt7w%3D&md5=598be259df18540fc4f17627ae5de13dCAS |

Dallai, R. (1979). Investigations on Collembola. XXIV. On the systematic of Neelidae with redescription of Neelides folsomi Caroli. Animalia 6, 271–281.

Dányi, L. (2011). Cave dwelling springtails (Collembola) of Hungary: a review. Soil Organisms 83, 419–432.

Deharveng, L. (1978). Collemboles cavernicoles. 1. – Grottes de l’Aguzou (France: Aude). Extrait du Bulletin de la Société d’Histoire Naturelle de Toulouse 114, 393–403.

Deharveng, L., and Beruete, E. (1993). Megalothorax tubercularus n. sp., nouveau troglobie des Pyrénées-Atlantiques (France) et de Navarre (Espagne) (Collembola, Neelidae). Bulletin de la Societe Entomologique de France 98, 15–18.

Delamare Deboutteville, C., and Massoud, Z. (1962). Collemboles Symphypléones. In ‘Biologie de l’Amérique Australe. Volume II’. (Ed. CNRS.) pp. 169–289.

Denis, J. R. (1948). Collemboles d’Indochine. Notes d’Entomologie chinoise. Musée Heude 12, 183–311.

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=fb309fc886ca0bad32dc0daac67aa1f7CAS | 15034147PubMed |

Ekrem, T., Willassen, E., and Stur, E. (2007). A comprehensive DNA sequence library is essential for identification with DNA barcodes. Molecular Phylogenetics and Evolution 43, 530–542.
A comprehensive DNA sequence library is essential for identification with DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1altrk%3D&md5=db19f0b61109e2e04a9048f16b907549CAS | 17208018PubMed |

Fjellberg, A. (1998). The labial palp in Collembola. Zoologischer Anzeiger 237, 309–330.

Fjellberg, A. (2007). Collembola of Fennoscandia and Denmark. Part II: Entomobryomorpha and Symphypleona. Fauna Entomologica Scandinavia 42, 1–264.

Folsom, J. W. (1901). Review of the Collembolan genus Neelus and description of N. minutus n. sp. Psyche 9, 219–222.

García-Gómez, A., Castaño-Meneses, G., and Palacios-Vargas, J. G. (2009). Diversity of springtails (Hexapoda) according to a altitudinal gradient. Pesquisa Agropecuaria Brasileira 44, 911–916.
Diversity of springtails (Hexapoda) according to a altitudinal gradient.Crossref | GoogleScholarGoogle Scholar |

Giribet, G. (2003). Stability in phylogenetic formulations and its relationship to nodal support Systematic Biology 52, 554–564.
| 12857646PubMed |

Gisin, H. (1960). ‘Collembolenfauna Europas.’ pp. 1–312. (Muséum d’Histoire Naturelle, Genève.)

Goloboff, P. A. (1999). Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15, 415–428.
Analyzing large data sets in reasonable times: solutions for composite optima.Crossref | GoogleScholarGoogle Scholar |

Goloboff, P. A., Farris, J. S., and Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786.
TNT, a free program for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |

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 |

Hajibabaei, M., Singer, G. A., Hebert, P. D., and Hickey, D. A. (2007). DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics 23, 167–172.
DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjslShur8%3D&md5=b5193ecd8f7499692507ee71bd824376CAS | 17316886PubMed |

Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=a58e8054c576c226425e8c119c083c16CAS |

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 | 1:CAS:528:DC%2BD2cXovVyju7g%3D&md5=c5367a30163d4a7e036d6fcd4de51647CAS |

Hüther, W. (1967). Beiträge zur Kenntnis der Collembolenfauna des Sudans. II. Allgemeiner Teil und Symphypleona. Senckenbergiana Biologica 48, 221–267.

Janies, D. (2001). Phylogenetic relationships of extant echinoderm classes. Canadian Journal of Zoology 79, 1232–1250.
Phylogenetic relationships of extant echinoderm classes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsVOltb8%3D&md5=534175d13e106afbe0a0ecbc4db29f5cCAS |

Kováč, L., and Papáč, V. (2010). Revision of the genus Neelus Folsom, 1896 (Collembola, Neelida) with the description of two new troglobiotic species from Europe. Zootaxa 2663, 36–52.

Lanfear, R., Calcott, B., and Ho, S. Y. W. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=efb70362a95ef9b6dfffd82935ae7e98CAS | 22319168PubMed |

Loranger, G., Bandyopadhyaya, I., Razaka, B., and Ponge, J.-F. (2001). Does soil acidity explain altitudinal sequences in collembolan communities? Soil Biology & Biochemistry 33, 381–393.
Does soil acidity explain altitudinal sequences in collembolan communities?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslKlsLo%3D&md5=255e121b5026616f828d147c474a1685CAS |

Massoud, Z. (1971). Contribution à la connaissance morphologique et systématique des collemboles Neelidae. Revue d’Ecologie et de Biologie du Sol 8, 195–198.

Massoud, Z., and Vannier, G. (1965). Megalothorax gabonensis, n. sp. et discussion sur la griffe des Neelidae. Revue d’Ecologie et de Biologie du Sol 2, 229–237.

Maynard, E. A. (1951). ‘A Monograph of the Collembola or Springtail Insects of New York State.’ pp. 1–339. (Ithaca, New York.)

Mickevich, M. F., and Farris, J. S. (1981). The implications of congruence in Menidia. Systematic Zoology 30, 351–370.

Nixon, K. C. (1999). The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15, 407–414.
The parsimony ratchet, a new method for rapid parsimony analysis.Crossref | GoogleScholarGoogle Scholar |

Palacios-Vargas, J. G., and Sánchez, A. (1999). Nuevas especies de Megalothorax (Collembola: Neelidae) de cuevas mexicanas. Folia Entomologica Mexicana 105, 55–64.

Rapoport, E. H. (1962). Colémbolos de Bahía Blanca (Argentina) III. Publicaciones del Institutode Edafología E Hidrología 2, 3–24.

Rusek, J. (1987). New types of linea ventralis in Collembola and its function. In ‘Soil fauna and soil fertility. Proceedings of the 9th International Colloquium on Soil Zoology’. (Ed. W. Striganova.) pp. 699–706. (Moscow.)

Salmon, J. T. (1946). Collembola – Symphypleona from the Homer district. Dominion Museum Records in Entomology 1, 27–61.

Salmon, J. T. (1964). An index to the Collembola. Royal Society of New Zealand Bulletin 7, 145–644.

Saunders, G. W., and McDonald, B. (2010). DNA barcoding reveals multiple overlooked Australian species of the red algal order Rhodymeniales (Florideophyceae), with resurrection of Halopeltis J. Agardh and description of Pseudohalopeltis gen. nov. Botany 88, 639–667.
DNA barcoding reveals multiple overlooked Australian species of the red algal order Rhodymeniales (Florideophyceae), with resurrection of Halopeltis J. Agardh and description of Pseudohalopeltis gen. nov.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1yjurk%3D&md5=f756f383f78547fc01cdd6f432019e9aCAS |

Schneider, C., Cruaud, C., and D’Haese, C. A. (2011). Unexpected diversity in Nelipleona revealed by molecular phylogeny approach (Hexapoda, Collembola). Soil Organisms 83, 383–398.

Stach, J. (1957). ‘The Apterygotan Fauna of Poland in Relation to the World-Fauna of this Group of Insects. Families: Neelidae and Dicyrtomidae.’ pp. 1–113. (Polska Akademia Nauk: Kraków, Poland.)

Stach, J. (1960). Materialen zur kenntis der collembolen fauna Afghanistans. In ‘Contribution à l’étude de la faune d’Afghanistan. Vol. 45’. Acta Zoologica Cracoviensia 5, 507–581.

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=b75cb342275b0257cdc9a3a5e1c1c37bCAS | 16928733PubMed |

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.

Suetsugu, N., Satoh, F., and Koike, T. (2010). An atlas of Collembola species in the Sapporo Experimental Forest of Hokkaido University in Northern Japan. Eurasian Journal of Forest Research 13, 57–67.

Vannier, G., and Massoud, Z. (1967). Productions cireuses chez les Collemboles Neelidae. Revue d’Écologie et de Biologie du Sol 4, 123–130.

Varón, A., Vinh, L. S., and Wheeler, W. C. (2010). POY version 4: phylogenetic analysis using dynamic homologies. Cladistics 26, 72–85.
POY version 4: phylogenetic analysis using dynamic homologies.Crossref | GoogleScholarGoogle Scholar |

Wheeler, W. C. (1995). Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. Systematic Biology 44, 321–331.

Wheeler, W. C. (1996). Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12, 1–9.
Optimization alignment: the end of multiple sequence alignment in phylogenetics?Crossref | GoogleScholarGoogle Scholar |

Wheeler, W. C. (2003). Iterative pass optimization of sequence data. Cladistics 19, 254–260.
Iterative pass optimization of sequence data.Crossref | GoogleScholarGoogle Scholar | 12901382PubMed |

Willem, V. (1900). Un type nouveau de Sminthuride: Megalothorax. Annales de la Société Entomologique de Belgique 44, 7–10.

Womersley, H. (1932). The Collembola–Symphypleona of Australia: a preliminary account. Commonwealth of Australia Council for Scientific and Industrial Research 34, 1–47.

Yosii, R. (1976). Structure and chaetotaxy of labrum as the taxonomic character of Collembola. Revue d’Écologie et de Biologie du Sol 13, 233–239.