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

The aberrant millipede genus Pteridoiulus and its position in a revised molecular phylogeny of the family Julidae (Diplopoda : Julida)

Henrik Enghoff A B , Gitte Petersen A and Ole Seberg A
+ Author Affiliations
- Author Affiliations

A Natural History Museum of Denmark, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark.

B Corresponding author. Email: henghoff@snm.ku.dk

Invertebrate Systematics 27(5) 515-529 https://doi.org/10.1071/IS13016
Submitted: 12 April 2013  Accepted: 8 September 2013   Published: 31 October 2013

Abstract

A phylogenetic analysis of 62 species (32 genera) of the Palaearctic millipede family Julidae, including the aberrant alpine genus Pteridoiulus Verhoeff, 1913, was made based on partial sequences of the mitochondrial 16S rRNA (16S) gene and the nuclear 28S rRNA (28S) gene, respectively. The two datasets (16S rDNA and 28S rDNA) were analysed in combination but treated as different partitions using direct optimisation as implemented in POY. The 16S rDNA and the 28S rDNA sequences vary from 410 to 449 bp and from 467 to 525 bp in length, respectively. All searches were performed under six different gap opening costs, an extension gap cost of 1, and a substitution cost of 2. Based on previous investigations the optimal gap opening cost was set to 4, and the robustness of different gap opening costs ranging from 1 to 6 investigated. Additionally, the two data partitions were aligned individually using MAFTT and run in TNT both with gaps treated as a fifth state, and as missing, and finally the alignments were used as input in a maximum likelihood (ML) analysis. The order Julida and the family Julidae were recovered as monophyletic under all weight sets in POY, as well as in the TNT and ML analyses. Likewise, in all analyses Pteridoiulus was found to be sister to another monotypic alpine genus, Heteroiulus Verhoeff, 1897. The Pteridoiulus + Heteroiulus clade is robust to parameter changes but lacks morphological support. The distribution pattern of the clade, Pteridoiulus in the eastern Alps (mainly Austria), Heteroiulus in the southern Alps (Italy) seems unique, since similar patterns all involve very similar, closely related species pairs.


References

Aagesen, L., Petersen, G., and Seberg, O. (2005). Sequence length variation, indel costs, and congruence in sensitivity analysis. Cladistics 21, 15–30.
Sequence length variation, indel costs, and congruence in sensitivity analysis.Crossref | GoogleScholarGoogle Scholar |

Akkari, N., and Enghoff, H. (2012). Review of the genus Ommatoiulus in Andalusia, Spain (Diplopoda: Julida) with description of ten new species and notes on a remarkable gonopod structure, the fovea. Zootaxa 3538, 1–53.

Akkari, N., Stoev, P., and Enghoff, H. (2011). Two new cavernicolous genera of Julidae (Diplopoda: Julida), with notes on the tribe Brachyiulini and on julid subanal hooks and anchors. ZooKeys 114, 13–34.
Two new cavernicolous genera of Julidae (Diplopoda: Julida), with notes on the tribe Brachyiulini and on julid subanal hooks and anchors.Crossref | GoogleScholarGoogle Scholar |

Akkari, N., Enghoff, H., Cheung, D. K.-B., and Stoev, P. (2013). Revolving SEM images visualising 3D taxonomic characters – application to five new species of the millipede genus Ommatoiulus Latzel, 1884 with an interactive key to the Ommatoiulus species of Tunisia (Diplopoda, Julida, Julidae). ZooKeys 328, 5–45.
| 24146546PubMed |

Attems, C. (1949). Die Myriopodenfauna der Ostalpen. Sitzungsberichte der Akademie der Wissenschaften in Wien, mathematisch-naturwissenschaftliche Klasse 158, 79–153.

Attems, C. (1954). Myriapoda. In: ‘Die Nordost-Alpen im Spiegel ihrer Landtierwelt I’. (Ed. H. Franz.) pp. 288–328. (Universitätsverlag Wagner: Innsbruck, Austria.)

Brewer, M. S., Sierwald, P., and Bond, J. E. (2012). Millipede taxonomy after 250 years: classification and taxonomic practices in a mega-diverse yet understudied arthropod group. PLoS ONE 7, e37240.
Millipede taxonomy after 250 years: classification and taxonomic practices in a mega-diverse yet understudied arthropod group.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnslyhtrY%3D&md5=e5b3d8310b11e7c3e53ab8eb8017949dCAS | 22615951PubMed |

Cognato, A. I., and Vogler, A. P. (2001). Exploring data interaction and nucleotide alignment in a multiple gene analysis of Ips (Coleoptera: Scolytidae). Systematic Biology 50, 758–780.
Exploring data interaction and nucleotide alignment in a multiple gene analysis of Ips (Coleoptera: Scolytidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntVKmtA%3D%3D&md5=8e96d3d3183dd27f2dd1acfde186e047CAS | 12116633PubMed |

Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research Jul 1; 36 (web server issue): W465–9.

Enghoff, H. (1981). A cladistic analysis and classification of the millipede order Julida. Journal of Zoological Systematics and Evolutionary Research 19, 285–319.

Enghoff, H. (1987). Revision of Nepalmatoiulus Mauries 1983 – a southeast Asiatic genus of millipedes (Diplopoda: Julida: Julidae). Courier Forschungs-Institut Senckenberg 93, 241–331.

Enghoff, H. (1991). A revised cladistic analysis and classification of the millipede order Julida. With establishment of four new families and description of a new nemasomatoid genus from Japan. Journal of Zoological Systematics and Evolutionary Research 29, 241–263.
A revised cladistic analysis and classification of the millipede order Julida. With establishment of four new families and description of a new nemasomatoid genus from Japan.Crossref | GoogleScholarGoogle Scholar |

Enghoff, H. (1995). A revision of the Paectophyllini and Calyptophyllini: millipedes of the Middle East (Diplopoda, Julida, Julidae). Journal of Natural History 29, 685–786.
A revision of the Paectophyllini and Calyptophyllini: millipedes of the Middle East (Diplopoda, Julida, Julidae).Crossref | GoogleScholarGoogle Scholar |

Enghoff, H. (1996). The penis as a phylogenetic character in the millipede family Julidae. Mémoires du Muséum national d’Histoire naturelle, Paris 169, 313–326.

Enghoff, H. (2012). Three new species of Dolichoiulus millipedes from the underground of Gran Canaria, with notes on the circumscription of the genus (Diplopoda, Julida, Julidae). European Journal of Taxonomy 15, 1–12.

Enghoff, H., Petersen, G., and Seberg, O. (2011). Phylogenetic relationships in the millipede family Julidae. Cladistics 27, 606–616.
Phylogenetic relationships in the millipede family Julidae.Crossref | GoogleScholarGoogle Scholar |

Gantenbein, B., Fet, V., Barker, M., and Scholl, A. (2000). Nuclear and mitochondrial markers reveal the existence of two parapatric scorpion species in the Alps: Euscorpius germanus (C.L. Koch, 1837) and E. alpha Caporicaco, 1950, stat. nov. (Euscorpiidae). Revue Suisse de Zoologie 107, 843–869.

Giribet, G., and Wheeler, W. C. (1999). On gaps. Molecular Phylogenetics and Evolution 13, 132–143.
On gaps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1Omsbs%3D&md5=66babcf626eab1b4ae84c4c40fa7d648CAS | 10508546PubMed |

Goloboff, P. A., and Catalano, S. A. (2012). GB-to-TNT: facilitating creation of matrices from GenBank and diagnosis of results in TNT. Cladistics 28, 503–513.
GB-to-TNT: facilitating creation of matrices from GenBank and diagnosis of results in TNT.Crossref | GoogleScholarGoogle Scholar |

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

Golovatch, S. I., Geoffroy, J.-J., Mauriès, J.-P., and VandenSpiegel, D. (2012). New and poorly-known species of the millipede genus Trachyjulus Peters, 1864 (Diplopoda, Spirostreptida, Cambalopsidae). Arthropoda Selecta 21, 103–129.

Gruber, J. (2009). Diplopoda (Doppelfüsser). In ‘Endemiten – Kostbarkeiten in Österreichs Pflanzen – und Tierwelt’. (Eds W. Rabitsch and F. Essl.) pp. 512–541. (Naturwissenschaftlicher Verein für Kärnten und Umweltbundesamt GmbH: Klagenfurtand Wien, Austria.)

Hoffman, R. L. (1980, for 1979) ‘Classification of the Diplopoda.’ (Muséum d’Histoire Naturelle: Genève, Switzerland.)

Kime, R. D., and Enghoff, H. (in prep.). ‘Atlas of European Millipedes (Class Diplopoda), Volume 2, Order Julida.’ Fauna Europaea Evertebrata (Pensoft: Sofia, Moscow.)

Korge, H. (1976). Beitrage zur Kenntnis des Wimbachgriestales im Naturschutzgebiet Konigssee bei Berchtesgaden. Verhandlungen des Botanischen Vereins der Provinz Brandenburg 112, 131–160.

Lazányi, E., and Vagalinski, B. (). Redefinition of the millipede subgenus Megaphyllum sensu stricto Verhoeff, 1894 and neotype designation for Megaphyllum austriacum (Latzel, 1884) (Myriapoda: Diplopoda: Julida: Julidae). Zootaxa. , .

Lazányi, E., Vagalinski, B., and Korsós, Z. (2012). The millipede genus Megaphyllum Verhoeff, 1894 in the Balkan Peninsula, with description of new species (Myriapoda: Diplopoda: Julida: Julidae). Zootaxa 3228, 1–47.

Lohmander, H. (1936). Die Diplopoden des Kaukasus-Gebietes. Göteborgs Kungliga vetenskaps-och vitterhets-Samhällets Handlingar, 5. Följden. Ser. B 5, 1–196.

Martens, J. (1969). Die Abgenzung von Biospezies auf biologisch-ethologischer und morphologischer Grundlage am Beispiel der Gattung Ischyropsalis C.L. Koch 1839 (Opiliones, Ischyropsalididae). Zoologische Jahrbucher. Abteilung fur Systematik, Ökologie und Geographie der Tiere 96, 133–264.

Muraji, M., and Tachikawa, S. (2000). Phylogenetic analysis of water striders (Hemiptera: Gerroidea) based on partial sequences of mitochondrial and nuclear ribosomal RNA genes. Entomological Science 3, 611–615.

Petersen, G., Seberg, O., Aagesen, L., and Frederiksen, S. (2004). An empirical test of the treatment of indels during optimization alignment based on the phylogeny of the genus Secale (Poaceae). Molecular Phylogenetics and Evolution 30, 733–742.
An empirical test of the treatment of indels during optimization alignment based on the phylogeny of the genus Secale (Poaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFWhsA%3D%3D&md5=ab89b8ab962ef5e81f43689b0adc342bCAS | 15012951PubMed |

Petersen, G., Knudsen, H., and Seberg, O. (2010). Alignment, clade robustness and fungal phylogenetics – Crepidotaceae and sister families revisited. Cladistics 26, 62–71.
Alignment, clade robustness and fungal phylogenetics – Crepidotaceae and sister families revisited.Crossref | GoogleScholarGoogle Scholar |

Phillips, A., Janies, D., and Wheeler, W. (2000). Multiple sequence alignment in phylogenetic analysis Molecular Phylogenetics and Evolution 16, 317–330.
Multiple sequence alignment in phylogenetic analysisCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsV2nurg%3D&md5=53e6fcb867cc10539d88f706c3963bbaCAS | 10991785PubMed |

Read, H. J. (1990). The generic composition and relationships of the Cylindroiulini – a cladistic analysis (Diplopoda, Julida: Julidae). Entomologica Scandinavica 21, 97–112.
The generic composition and relationships of the Cylindroiulini – a cladistic analysis (Diplopoda, Julida: Julidae).Crossref | GoogleScholarGoogle Scholar |

Reip, H. E., Decker, P., Voigtlander, K., Lindner, E. N., Hannig, K., and Spelda, J. (2012). Seltene Myriapoden Deutschlands (Diplopoda, Chilopoda). Schubartiana 5, 49–112.

Schönswetter, P., Tribsch, A., Schneeweiss, G. M., and Niklfeld, H. (2003). Disjunctions in relict alpine plants: phylogeography of Androsace brevis and A. wulfeniana (Primulaceae). Botanical Journal of the Linnean Society 141, 437–446.
Disjunctions in relict alpine plants: phylogeography of Androsace brevis and A. wulfeniana (Primulaceae).Crossref | GoogleScholarGoogle Scholar |

Schubart, O. (1934). Tausendfüßler oder Myriapoda I: Diplopoda. Die Tierwelt Deutschlands 28, 1–318.

Sierwald, P., and Bond, J. E. (2007). Current status of the myriapod class Diplopoda (millipedes): taxonomic diversity and phylogeny. Annual Review of Entomology 52, 401–420.
Current status of the myriapod class Diplopoda (millipedes): taxonomic diversity and phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWms7s%3D&md5=bbc65f0975ac0cc28da54bc8bc812b2fCAS | 17163800PubMed |

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
| 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=f9162bafe571abe5c8b8b4f7c3d5d941CAS |

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 |

Strasser, K. (1940). Diplopoden des jugoslavischen Draubanats. Prirodoslovne Razprave 4, 13–85.

Thaler, K., de Zordo, I., Meyer, E., Schatz, H., and Troger, H. (1978). Arthropoden auf Almflächen im Raum von Badgastein (Zentralalpen, Salzburg, Österreich). Veröffentlichungen des österreichischen MaB-Hochgebirgsprogramms Hohe Tauern 2, 195–233.

Varón, A., Vinh, L. S., Bomash, I., and Wheeler, W. C. (2007). ‘POY 4.1.2.1. Program Documentation.’ (American Museum of Natural History: New York, USA.)

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 |

Verhoeff, K. W. (1913). Zwei neue Iuliden-gattungen aus den Tauern. Zoologischer Anzeiger 43, 145–161.

Verhoeff, K. W. (1928). Klasse Diplopoda 1. Bronn, H. G. Klassen und Ordnungen des Tierreichs 5, 1–1072.

Verhoeff, K. W. (1932). Klasse Diplopoda 2. Teil. Bronn’s Klassen und Ordnungen des Tierreichs 5, 1073–2084.

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 |