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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

A new species of Tithaeidae (Arachnida: Opiliones: Laniatores) from Mindanao reveals contemporaneous colonisation of the Philippines by Sunda Shelf opiliofauna

Stephanie M. Schmidt A , Perry A. C. Buenavente B , Darrell D. Blatchley C , Arvin C. Diesmos B , Mae L. Diesmos B , David Emmanuel M. General D , Alma B. Mohagan E , Dale Joy Mohagan E , Ronald M. Clouse F and Prashant P. Sharma https://orcid.org/0000-0002-2328-9084 A G
+ Author Affiliations
- Author Affiliations

A Department of Integrative Biology, University of Madison-Wisconsin, 352 Birge Hall, 430 Lincoln Drive, Madison, WI 53706, USA.

B Herpetology Section, Zoology Division, National Museum of Natural History of the Philippines, Teodoro F. Valencia Circle, Ermita 1000, Manila, Philippines.

C D’Bone Collector Museum, San Pedro St., Poblacion District, Bucana Barangay 76-A, Davao City, Minadanao, Philippines.

D University of the Philippines Los Baños Museum of Natural History, College, Los Baños, Laguna 4031, Philippines.

E Biology Department, Central Mindanao University, University Town, Musuan, 8710 Bukidnon, Philippines.

F Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York City, NY 10024, USA.

G Corresponding author. Email: prashant.sharma@wisc.edu

Invertebrate Systematics 33(1) 237-251 https://doi.org/10.1071/IS18057
Submitted: 15 July 2018  Accepted: 8 October 2018   Published: 6 February 2019

Abstract

The Philippine archipelago harbours a remarkable diversity of harvestmen, with respect to both taxonomy and complexity of biogeographic origins. Among the armoured harvestmen (suborder Laniatores), six families of distantly related groups occur in this archipelago. Here, we describe a new species of the family Tithaeidae, Tithaeus odysseus sp. nov., discovered during a collecting campaign on the island of Mindanao. The description of this species expands the known distribution of the family and demonstrates another exception to the zoogeographic boundary known as Huxley’s Line which putatively separates the biota of the Philippines (excluding the Palawan island group) from the Sunda Shelf biota. Given the coincident distributions of Tithaeidae and the mite harvestman family Stylocellidae (Cyphophthalmi), a group renowned for its poor dispersal ability, we inferred phylogenetic relationships and divergence times of the Philippines lineages of both families by using a comprehensive molecular dating analysis of all Opiliones. The internal phylogeny of Tithaeidae mirrored the biogeography of Philippine Stylocellidae, showing a close affinity between the Philippine and Bornean species. Molecular dating showed contemporaneous colonisation of Mindanao by both families in the Cretaceous. We infer these patterns to reflect faunal connections between the southern Philippines and Borneo via the Zamboanga Peninsula. To render the genus Tithaeus monophyletic, we synonymise Metatithaeus with Tithaeus (new synonymy).

Additional keywords: comparative biogeography, Cyphophthalmi, Epedanoidea, Grassatores, Southeast Asia.


References

Boyer, S. L., and Giribet, G. (2007). A new model Gondwanan taxon: systematics and biogeography of the harvestman family Pettalidae (Arachnida, Opiliones, Cyphophthalmi), with a taxonomic revision of genera from Australia and New Zealand. Cladistics 23, 337–361.
A new model Gondwanan taxon: systematics and biogeography of the harvestman family Pettalidae (Arachnida, Opiliones, Cyphophthalmi), with a taxonomic revision of genera from Australia and New Zealand.Crossref | GoogleScholarGoogle Scholar |

Boyer, S. L., Clouse, R. M., Benavides, L. R., Sharma, P., Schwendinger, P. J., Karunarathna, I., and Giribet, G. (2007). Biogeography of the world: a case study from cyphophthalmid Opiliones, a globally distributed group of arachnids. Journal of Biogeography 34, 2070–2085.
Biogeography of the world: a case study from cyphophthalmid Opiliones, a globally distributed group of arachnids.Crossref | GoogleScholarGoogle Scholar |

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 | 10742046PubMed |

Clouse, R. M., and Giribet, G. (2007). Across Lydekker’s Line–first report of mite harvestmen (Opiliones: Cyphophthalmi: Stylocellidae) from New Guinea. Invertebrate Systematics 21, 207–227.
Across Lydekker’s Line–first report of mite harvestmen (Opiliones: Cyphophthalmi: Stylocellidae) from New Guinea.Crossref | GoogleScholarGoogle Scholar |

Clouse, R. M., and Giribet, G. (2010). When Thailand was an island: the phylogeny and biogeography of mite harvestmen (Opiliones, Cyphophthalmi, Stylocellidae) in Southeast Asia. Journal of Biogeography 37, 1114–1130.
When Thailand was an island: the phylogeny and biogeography of mite harvestmen (Opiliones, Cyphophthalmi, Stylocellidae) in Southeast Asia.Crossref | GoogleScholarGoogle Scholar |

Clouse, R. M., General, D. M., Diesmos, A. C., and Giribet, G. (2011). An old lineage of Cyphophthalmi (Opiliones) discovered on Mindanao highlights the need for biogeographical research in the Philippines. The Journal of Arachnology 39, 147–153.
An old lineage of Cyphophthalmi (Opiliones) discovered on Mindanao highlights the need for biogeographical research in the Philippines.Crossref | GoogleScholarGoogle Scholar |

Diamond, J. M., and Gilpin, M. E. (1983). Biogeographic umbilici and the origin of the Philippine avifauna. Oikos 41, 307–321.

Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214–218.
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |

Drummond, A. J., Ho, S. Y. W., Phillips, M. J., and Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.
Relaxed phylogenetics and dating with confidence.Crossref | GoogleScholarGoogle Scholar | 16683862PubMed |

Dunlop, J. A., Anderson, L. I., Kerp, H., and Hass, H. (2003). Preserved organs of Devonian harvestmen. Nature 425, 916.
Preserved organs of Devonian harvestmen.Crossref | GoogleScholarGoogle Scholar | 14586459PubMed |

Dunlop, J., Anderson, L., Kerp, H., and Hass, H. (2004). A harvestman (Arachnida: Opiliones) from the Early Devonian Rhynie cherts, Aberdeenshire, Scotland. Transactions of the Royal Society of Edinburgh. Earth Sciences 94, 341–354.
A harvestman (Arachnida: Opiliones) from the Early Devonian Rhynie cherts, Aberdeenshire, Scotland.Crossref | GoogleScholarGoogle Scholar |

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 | 15034147PubMed |

Fernández, R., Sharma, P. P., Tourinho, A. L., and Giribet, G. (2017). The Opiliones tree of life: shedding light on harvestmen relationships through transcriptomics. Proceedings. Biological Sciences 284, 20162340.
The Opiliones tree of life: shedding light on harvestmen relationships through transcriptomics.Crossref | GoogleScholarGoogle Scholar | 28228511PubMed |

Garwood, R. J., Sharma, P. P., Dunlop, J. A., and Giribet, G. (2014). A Paleozoic stem group to mite harvestmen revealed through integration of phylogenetics and development. Current Biology 24, 1017–1023.
A Paleozoic stem group to mite harvestmen revealed through integration of phylogenetics and development.Crossref | GoogleScholarGoogle Scholar | 24726154PubMed |

Giribet, G., and Kury, A. B. (2007). Phylogeny and biogeography. In ‘Harvestmen: the biology of Opiliones’. (Eds R. Pinto-da-Rocha, G. Machado and G. Giribet.) pp. 62–87. (Harvard University Press: Cambridge, MA, USA.)

Giribet, G., and Sharma, P. P. (2015). Evolutionary biology of harvestmen (Arachnida, Opiliones). Annual Review of Entomology 60, 157–175.
Evolutionary biology of harvestmen (Arachnida, Opiliones).Crossref | GoogleScholarGoogle Scholar | 25341103PubMed |

Giribet, G., Sharma, P., and Bastawade, D. (2007). A new genus and species of Cyphophthalmi (Arachnida: Opiliones) from the north-eastern states of India. Biological Journal of the Linnean Society. Linnean Society of London 151, 663–670.
A new genus and species of Cyphophthalmi (Arachnida: Opiliones) from the north-eastern states of India.Crossref | GoogleScholarGoogle Scholar |

Giribet, G., Vogt, L., González, A. P., Sharma, P., and Kury, A. B. (2010). A multilocus approach to harvestman (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores. Cladistics 26, 408–437.
A multilocus approach to harvestman (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores.Crossref | GoogleScholarGoogle Scholar |

Giribet, G., Sharma, P. P., Benavides, L. R., Boyer, S. L., Clouse, R. M., de Bivort, B. L., Dimitrov, D., Kawauchi, G. Y., Murienne, J., and Schwendinger, P. J. (2012). Evolutionary and biogeographical history of an ancient and global group of arachnids (Arachnida: Opiliones: Cyphophthalmi) with a new taxonomic arrangement. Biological Journal of the Linnean Society. Linnean Society of London 105, 92–130.
Evolutionary and biogeographical history of an ancient and global group of arachnids (Arachnida: Opiliones: Cyphophthalmi) with a new taxonomic arrangement.Crossref | GoogleScholarGoogle Scholar |

Giribet, G., Boyer, S. L., Baker, C. M., Fernández, R., Sharma, P. P., de Bivort, B. L., Daniels, S. R., Harvey, M. S., and Griswold, C. E. (2016). A molecular phylogeny of the temperate Gondwanan family Pettalidae (Arachnida, Opiliones, Cyphophthalmi) and the limits of taxonomic sampling. Zoological Journal of the Linnean Society 178, 523–545.
A molecular phylogeny of the temperate Gondwanan family Pettalidae (Arachnida, Opiliones, Cyphophthalmi) and the limits of taxonomic sampling.Crossref | GoogleScholarGoogle Scholar |

Gouy, M., Guindon, S., and Gascuel, O. (2010). SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.
SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building.Crossref | GoogleScholarGoogle Scholar | 19854763PubMed |

Groh, S., and Giribet, G. (2014). Polyphyly of Caddoidea, reinstatement of the family Acropsopilionidae in Dyspnoi, and a revised classification system of Palpatores (Arachnida, Opiliones). Cladistics 31, 277–290.
Polyphyly of Caddoidea, reinstatement of the family Acropsopilionidae in Dyspnoi, and a revised classification system of Palpatores (Arachnida, Opiliones).Crossref | GoogleScholarGoogle Scholar |

Hall, R. (2002). Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Sciences 20, 353–431.
Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations.Crossref | GoogleScholarGoogle Scholar |

Hedin, M., Tsurusaki, N., Macías-Ordóñez, R., and Shultz, J. W. (2012). Molecular systematics of sclerosomatid harvestmen (Opiliones, Phalangioidea, Sclerosomatidae): geography is better than taxonomy in predicting phylogeny. Molecular Phylogenetics and Evolution 62, 224–236.
Molecular systematics of sclerosomatid harvestmen (Opiliones, Phalangioidea, Sclerosomatidae): geography is better than taxonomy in predicting phylogeny.Crossref | GoogleScholarGoogle Scholar | 22001211PubMed |

Jones, A. W., and Kennedy, R. S. (2008). Evolution in a tropical archipelago: comparative phylogeography of Philippine fauna and flora reveals complex patterns of colonization and diversification. Biological Journal of the Linnean Society 95, 620–639.

Kury, A. B. (1993). Análise filogenética de Gonyleptoidea (Arachnida, Opiliones, Laniatores). Ph.D. Thesis, Universidade de São Paulo, São Paulo, Brazil.

Kury, A. B. (2003). Annotated catalogue of the Laniatores of the New World (Arachnida, Opiliones). Revista Ibérica de Aracnología Volumen Especial Monográfico 1, 1–337.

Kury, A. B. (2006). ‘Checklist of valid genera of Opiliones of the World, Museu Nacional/UFRJ.’ Available at http://www. museunacional.ufrj.br/mndi/Aracnologia/checklaniator.htm/ [Verified 10 July 2018].

Lian, W.-G., Zhu, M.-S., and Kury, A. B. (2008). A new species of the genus Tithaeus from China (Arachnida: Laniatores: Epedanidae). Zootaxa 1841, 53–60.

Murienne, J., and Giribet, G. (2009). The Iberian Peninsula: ancient history of a hot spot of mite harvestmen (Arachnida: Opiliones: Cyphophthalmi: Sironidae) diversity. Zoological Journal of the Linnean Society 156, 785–800.
The Iberian Peninsula: ancient history of a hot spot of mite harvestmen (Arachnida: Opiliones: Cyphophthalmi: Sironidae) diversity.Crossref | GoogleScholarGoogle Scholar |

Murphree, C. S. (1988). Morphology of the dorsal integument of 10 opilionid species (Arachnida, Opiliones). The Journal of Arachnology 16, 237–252.

Oberski, J. T., Sharma, P. P., Jay, K. R., Coblens, M. J., Lemon, K. A., Johnson, J. E., and Boyer, S. L. (2018). A dated molecular phylogeny of mite harvestmen (Arachnida: Opiliones: Cyphophthalmi) elucidates ancient diversification dynamics in the Australian Wet Tropics. Molecular Phylogenetics and Evolution , .
A dated molecular phylogeny of mite harvestmen (Arachnida: Opiliones: Cyphophthalmi) elucidates ancient diversification dynamics in the Australian Wet Tropics.Crossref | GoogleScholarGoogle Scholar | 29935300PubMed |

Pérez González, A., and Kury, A. B. (2007). Samoidae Sørensen, 1886. In ‘Harvestmen: the biology of Opiliones’. (Eds R. Pinto-da-Rocha, G. Machado and G. Giribet.) pp. 224–226. (Harvard University Press: Cambridge, MA, USA.)

Poinar, G. (2009). Palaeosiro burmanicum n. gen. n. sp., a fossil Cyphophthalmi (Arachnida: Opiliones: Sironidae) in Early Cretaceous Burmese Amber. Monographs 12, 267–274.

Pubellier, M., Garcia, F., Loevenbruck, A., and Chorowicz, J. (2000). Recent deformation at the junction between the North Luzon block and the central Philippines from ERS-1 images. The Island Arc 9, 598–610.

Pubellier, M., Ali, J., and Monnier, C. (2003). Cenozoic plate interaction of the Australia and Philippine Sea Plates: ‘hit-and-run’ tectonics. Tectonophysics 363, 181–199.
Cenozoic plate interaction of the Australia and Philippine Sea Plates: ‘hit-and-run’ tectonics.Crossref | GoogleScholarGoogle Scholar |

Pubellier, M., Monnier, C., Maury, R., and Tamayo, R. (2004). Plate kinematics, origin and tectonic emplacement of supra-subduction ophiolites in SE Asia. Tectonophysics 392, 9–36.
Plate kinematics, origin and tectonic emplacement of supra-subduction ophiolites in SE Asia.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A., and Drummond, A. J. (2009). ‘Tracer v. 1.7.’ Program and documentation. Available at http://tree.bio.ed.ac.uk/software/tracer/ [Verified 10 July 2018].

Schönhofer, A. L., Vernesi, C., Martens, J., and Hedin, M. (2015). Molecular phylogeny, biogeographic history, and evolution of cave-dwelling taxa in the European harvestman genus Ischyropsalis (Opiliones: Dyspnoi). The Journal of Arachnology 43, 40–53.
Molecular phylogeny, biogeographic history, and evolution of cave-dwelling taxa in the European harvestman genus Ischyropsalis (Opiliones: Dyspnoi).Crossref | GoogleScholarGoogle Scholar |

Selden, P. A., Dunlop, J. A., Giribet, G., Zhang, W., and Ren, D. (2016). The oldest armoured harvestman (Arachnida: Opiliones: Laniatores), from Upper Cretaceous Myanmar amber. Cretaceous Research 65, 206–212.
The oldest armoured harvestman (Arachnida: Opiliones: Laniatores), from Upper Cretaceous Myanmar amber.Crossref | GoogleScholarGoogle Scholar |

Sharma, P. P. (2012). New Australasian Zalmoxidae (Opiliones: Laniatores) and a new case of male polymorphism in Opiliones. Zootaxa 3236, 1–35.

Sharma, P., and Giribet, G. (2005). A new Troglosiro species (Opiliones, Cyphophthalmi, Troglosironidae) from New Caledonia. Zootaxa 1053, 47–60.

Sharma, P., and Giribet, G. (2009a). A relict in New Caledonia: phylogenetic relationships of the family Troglosironidae (Opiliones: Cyphophthalmi). Cladistics 25, 25.

Sharma, P. P., and Giribet, G. (2009b). The family Troglosironidae (Opiliones: Cyphophthalmi) of New Caledonia. Mémoires du Muséum National d’Histoire Naturelle 198, 205–245.

Sharma, P., and Giribet, G. (2009c). Sandokanid phylogeny based on eight molecular markers. The evolution of a Southeast Asian endemic family of Laniatores (Arachnida, Opiliones). Molecular Phylogenetics and Evolution 52, 432–447.
Sandokanid phylogeny based on eight molecular markers. The evolution of a Southeast Asian endemic family of Laniatores (Arachnida, Opiliones).Crossref | GoogleScholarGoogle Scholar | 19324096PubMed |

Sharma, P. P., and Giribet, G. (2011). The evolutionary and biogeographic history of the armoured harvestmen – Laniatores phylogeny based on ten molecular markers, with the description of two new families of Opiliones (Arachnida). Invertebrate Systematics 25, 106–142.
The evolutionary and biogeographic history of the armoured harvestmen – Laniatores phylogeny based on ten molecular markers, with the description of two new families of Opiliones (Arachnida).Crossref | GoogleScholarGoogle Scholar |

Sharma, P. P., and Giribet, G. (2012). Out of the Neotropics: Late Cretaceous colonization of Australasia by American arthropods. Proceedings. Biological Sciences 279, 3501–3509.
Out of the Neotropics: Late Cretaceous colonization of Australasia by American arthropods.Crossref | GoogleScholarGoogle Scholar | 22628468PubMed |

Sharma, P. P., and Giribet, G. (2014). A revised dated phylogeny of the arachnid order Opiliones. Frontiers in Genetics 5, 255.
A revised dated phylogeny of the arachnid order Opiliones.Crossref | GoogleScholarGoogle Scholar | 25120562PubMed |

Sharma, P. P., Prieto, C., and Giribet, G. (2011a). A new family of Laniatores (Arachnida: Opiliones) from the Afrotropics. Invertebrate Systematics 25, 143–154.
A new family of Laniatores (Arachnida: Opiliones) from the Afrotropics.Crossref | GoogleScholarGoogle Scholar |

Sharma, P. P., Kury, A., and Giribet, G. (2011b). Zalmoxidae (Arachnida: Opiliones: Laniatores) of the Paleotropics: a catalogue of Southeast Asian and Indo-Pacific species. Zootaxa 2972, 37–58.

Sharma, P. P., Buenavente, P. A., Clouse, R. M., Diesmos, A. C., and Giribet, G. (2012). Forgotten gods: Zalmoxidae of the Philippines and Borneo (Opiliones: Laniatores). Zootaxa 3280, 29–55.

Sharma, P. P., Kaluziak, S. T., Perez-Pórro, A. R., Gonzalez, V. L., Hormiga, G., Wheeler, W. C., and Giribet, G. (2014). Phylogenomic interrogation of Arachnida reveals systemic conflicts in phylogenetic signal. Molecular Biology and Evolution 31, 2963–2984.
Phylogenomic interrogation of Arachnida reveals systemic conflicts in phylogenetic signal.Crossref | GoogleScholarGoogle Scholar | 25107551PubMed |

Sharma, P. P., Santiago, M. A., Kriebel, R., Lipps, S. M., Buenavente, P. A. C., Diesmos, A. C., Janda, M., Boyer, S. L., Clouse, R. M., and Wheeler, W. C. (2017). A multilocus phylogeny of Podoctidae (Arachnida, Opiliones, Laniatores) and parametric shape analysis reveal the disutility of subfamilial nomenclature in armored harvestman systematics. Molecular Phylogenetics and Evolution 106, 164–173.
A multilocus phylogeny of Podoctidae (Arachnida, Opiliones, Laniatores) and parametric shape analysis reveal the disutility of subfamilial nomenclature in armored harvestman systematics.Crossref | GoogleScholarGoogle Scholar | 27664345PubMed |

Shear, W. (1993a). The genus Troglosiro and the new family Troglosironidae (Opiliones, Cyphophthalmi). The Journal of Arachnology 21, 81–90.

Shear, W. (1993b). New species in the opilionid genus Stylocellus from Malaysia, Indonesia and the Philippines (Opiliones, Cyphophthahni, Stylocellidae). Bulletin of the British Arachnological Society 9, 174–188.

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 |

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML web servers.Crossref | GoogleScholarGoogle Scholar | 18853362PubMed |

Stelbrink, B., Albrecht, C., Hall, R., and von Rintelen, T. (2012). The biogeography of Sulawesi revisited: is there evidence for a vicariant origin of taxa on Wallace’s ‘anomalous island’? Evolution 66, 2252–2271.
The biogeography of Sulawesi revisited: is there evidence for a vicariant origin of taxa on Wallace’s ‘anomalous island’?Crossref | GoogleScholarGoogle Scholar | 22759300PubMed |

Suzuki, S. (1969). On a collection of opilionids from Southeast Asia. Journal of Science of the Hiroshima University 22, 11–77.

Yumul, G. P., Dimalanta, C. B., Marquez, E. J., and Queaño, K. L. (2009). Onland signatures of the Palawan microcontinental block and Philippine mobile belt collision and crustal growth process: a review. Journal of Asian Earth Sciences 34, 610–623.
Onland signatures of the Palawan microcontinental block and Philippine mobile belt collision and crustal growth process: a review.Crossref | GoogleScholarGoogle Scholar |

Zhang, C., and Zhang, F. (2010). A new Tithaeus species from Hainan Island, China (Arachnida, Opiliones, Laniatores, Epedanidae), with a key to the Chinese species. ZooKeys 67, 65–72.
A new Tithaeus species from Hainan Island, China (Arachnida, Opiliones, Laniatores, Epedanidae), with a key to the Chinese species.Crossref | GoogleScholarGoogle Scholar |