Integrative taxonomy reveals multiple lineages of the spider genus Cybaeus endemic to the Ryukyu Islands, Japan (Arachnida : Araneae : Cybaeidae)
Yoh Ihara A D , Naoki Koike B C and Takafumi Nakano B DA Hiroshima Environment & Health Association, 9-1 Hirose-kita-machi, Naka-ku, Hiroshima 730-8631, Japan.
B Department of Zoology, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.
C 982 Minamichitose-machi, Nagano 380-0822, Japan.
D Corresponding authors. Email: yoh.ihara@kanhokyo.or.jp; nakano@zoo.zool.kyoto-u.ac.jp
Invertebrate Systematics 35(2) 216-243 https://doi.org/10.1071/IS20070
Submitted: 11 September 2020 Accepted: 13 October 2020 Published: 8 February 2021
Abstract
The epigean spiders of the genus Cybaeus L. Koch, 1868 are known to have diversified in western North America and the Japanese Archipelago. To date, ~80 species of Cybaeus are known from Japan, but they have not previously been recorded from the Ryukyu Islands that harbour a diversity of endemic species. Here we describe eight new species of Cybaeus from the Ryukyu Islands, extending the range of Cybaeus southward to the central Ryukyus. Both sexes of each of the new species are described, and their phylogenetic relationships are estimated using nuclear and mitochondrial gene markers. Although Cybaeus okumurai, sp. nov. and C. kumadori, sp. nov. possess genital features that are common in the other Japanese congeners, the other six species (C. yakushimensis, sp. nov., C. kodama, sp. nov., C. amamiensis, sp. nov., C. aikana, sp. nov., C. tokunoshimensis, sp. nov., and C. hikidai, sp. nov.) are characterised by an elongated embolus and tubular spermathecae. These unique genital characteristics and the phylogeny recovered here suggest that these features evolved independently among the Japanese and Ryukyu Cybaeus species. Phylogenetic analyses highlight an unusual biogeographical pattern in which C. yakushimensis and C. kodama endemic to Yakushima Island in the northern Ryukyus are related to species distributed in the central Ryukyus. In contrast, our phylogeny suggests that C. okumurai from Tanegashima Island in the northern Ryukyus is sister to C. ashikitaensis (Komatsu, 1968), distributed in Kyushu of the Japanese Archipelago. The retreat constructs and sympatric distribution of Cybaeus found among the Ryukyus are also briefly discussed.
ZooBank: urn:lsid:zoobank.org:pub:640D15AA-17F4-48EE-88B4-485CFF8FCD60
Keywords: Arachnida, Araneae, Cybaeus, island fauna, morphology, phylogenetics, Ryukyu Islands, spider.
References
Bennett, R. G. (1985). The natural history and taxonomy of Cicurina bryantae Exline (Araneae, Agelenidae). The Journal of Arachnology 13, 87–96.Bennett, R. G. (1992). The spermathecal pores of spiders with special reference to dictynoids and amaurobioids (Araneae, Araneomorphae, Araneoclada). Proceedings of the Entomological Society of Ontario 123, 1–21.
Bennett, R. G. (2005). Cybaeidae. In ‘Spiders of North America: An Identification Manual’. (Eds D. Ubick, P. Paquin, P. E. Cushing, and V. Roth.) pp. 85–90. (American Arachnological Society: Greenville, SC, USA.)
Bennett, R. G. (2006). Ontogeny, variation, and synonymy in North American Cybaeus spiders (Araneae: Cybaeidae). Canadian Entomologist 138, 473–492.
| Ontogeny, variation, and synonymy in North American Cybaeus spiders (Araneae: Cybaeidae).Crossref | GoogleScholarGoogle Scholar |
Bennett, R. G. (2017). Cybaeidae. In ‘Spiders of North America: An Identification Manual’, 2nd edn. (Eds D. Ubick, P. Paquin, P. E. Cushing, and V. Roth.) pp. 96–101. (American Arachnological Society: Keene, NH, USA.)
Bennett, R., Copley, C., and Copley, D. (2016). Cybaeus (Araneae: Cybaeidae): the Nearctic species of the Holarctic clade. Zootaxa 4164, 1–67.
| Cybaeus (Araneae: Cybaeidae): the Nearctic species of the Holarctic clade.Crossref | GoogleScholarGoogle Scholar | 27701361PubMed |
Bennett, R., Copley, C., and Copley, D. (2019). Cybaeus (Araneae: Cybaeidae): the adenes species group of the Californian clade. Zootaxa 4711, 245–274.
| Cybaeus (Araneae: Cybaeidae): the adenes species group of the Californian clade.Crossref | GoogleScholarGoogle Scholar |
Bennett, R., Copley, C., and Copley, D. (2020). Allocybaeina littlewalteri (Araneae: Cybaeidae): a new genus and species endemic to northwestern California. Zootaxa 4845, 436–446.
| Allocybaeina littlewalteri (Araneae: Cybaeidae): a new genus and species endemic to northwestern California.Crossref | GoogleScholarGoogle Scholar |
Copley, C. R., Bennett, R., and Perlman, S. J. (2009). Systematics of Nearctic Cybaeus (Araneae: Cybaeidae). Invertebrate Systematics 23, 367–401.
| Systematics of Nearctic Cybaeus (Araneae: Cybaeidae).Crossref | GoogleScholarGoogle Scholar |
Ihara, Y. (2003). Cybaeus akiensis n. sp. (Araneae: Cybaeidae) from western Honshu, Japan, with some notes on its biology. Acta Arachnologica 52, 51–57.
| Cybaeus akiensis n. sp. (Araneae: Cybaeidae) from western Honshu, Japan, with some notes on its biology.Crossref | GoogleScholarGoogle Scholar |
Ihara, Y. (2004). Descriptions of large- and medium-sized species of the genus Cybaeus (Araneae: Cybaeidae) from the Tohoku district, northern Honshu, Japan. Acta Arachnologica 53, 35–51.
| Descriptions of large- and medium-sized species of the genus Cybaeus (Araneae: Cybaeidae) from the Tohoku district, northern Honshu, Japan.Crossref | GoogleScholarGoogle Scholar |
Ihara, Y. (2006). Cybaeus jinsekiensis n. sp., a spider species with protogynous maturation and mating plugs (Araneae: Cybaeidae). Acta Arachnologica 55, 5–13.
| Cybaeus jinsekiensis n. sp., a spider species with protogynous maturation and mating plugs (Araneae: Cybaeidae).Crossref | GoogleScholarGoogle Scholar |
Ihara, Y. (2008). ナミハグモ属の生殖器と体サイズにみられる地理的分化と種多様性 [Species diversity and geographic differentiations of reproductive organs and body size in the genus Cybaeus (Araneae: Cybaeidae) in Japan]. Acta Arachnologica 57, 87–109.
| ナミハグモ属の生殖器と体サイズにみられる地理的分化と種多様性 [Species diversity and geographic differentiations of reproductive organs and body size in the genus Cybaeus (Araneae: Cybaeidae) in Japan].Crossref | GoogleScholarGoogle Scholar |
Ihara, Y. (2009a). Cybaeidae. In ‘The Spiders of Japan: with Keys to the Families and Genera and Illustrations of the Species’. (Ed. H. Ono.) pp. 152–168. (Tokai University Press: Hadano, Japan.) [In Japanese].
Ihara, Y. (2009b). Revision of the Cybaeus hiroshimaensis-group (Araneae:Cybaeidae) in western Japan. Acta Arachnologica 58, 69–85.
| Revision of the Cybaeus hiroshimaensis-group (Araneae:Cybaeidae) in western Japan.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 | 23329690PubMed |
Kobayashi, T. (2006). Ten new species of the genus Cybaeus (Araneae: Cybaeidae) from central Honshu, Japan. Acta Arachnologica 55, 29–44.
| Ten new species of the genus Cybaeus (Araneae: Cybaeidae) from central Honshu, Japan.Crossref | GoogleScholarGoogle Scholar |
Komatsu, T. (1940). On five species of spiders found in the Ryugado Cave, Tosa Province. Acta Arachnologica 5, 186–195.
| On five species of spiders found in the Ryugado Cave, Tosa Province.Crossref | GoogleScholarGoogle Scholar |
Komatsu, T. (1961). ‘Cave Spiders of Japan, Their Taxonomy, Chorology and Ecology.’ (Arachnological Society of East Asia: Osaka, Japan.)
Komatsu, T. (1968). ‘Cave Spiders of Japan. II. Cybaeus, Dolichocybaeus and Heterocybaeus (Cybaeinae).’ (Arachnological Society of East Asia: Osaka, Japan.)
Komatsu, T., and Yaginuma, T. (1968). A new method for the observation of the spider genitalia. Acta Arachnologica 21, 34.
| A new method for the observation of the spider genitalia.Crossref | GoogleScholarGoogle Scholar |
Koressaar, T., and Remm, M. (2007). Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291.
| Enhancements and modifications of primer design program Primer3.Crossref | GoogleScholarGoogle Scholar | 17379693PubMed |
Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (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 | 22319168PubMed |
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2017). Partition Finder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| Partition Finder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 28013191PubMed |
Marusik, Y. M., and Kovblyuk, M. M. (2011). ‘Spiders (Arachnida, Aranei) of Siberia and Russian Far East.’ (KMK Scientific Press Ltd.: Moscow, Russia.) [In Russian].
Marusik, Y. M., and Logunov, D. V. (1991). Spiders of the superfamily Amaurobioidea (Aranei) from Sakhalin and Kurily Islands. Зоологический журнал 70, 87–94.
Matsuda, K., Ihara, Y., and Nakano, T. (2020). Description of a new species of Cybaeus (Araneae: Cybaeidae) from central Honshu, Japan. Species Diversity 25, 145–152.
| Description of a new species of Cybaeus (Araneae: Cybaeidae) from central Honshu, Japan.Crossref | GoogleScholarGoogle Scholar |
Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., and Lanfear, R. (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.
| IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era.Crossref | GoogleScholarGoogle Scholar | 32011700PubMed |
Motokawa, M. (2000). Biogeography of living mammals in the Ryukyu Islands. Tropics 10, 63–71.
| Biogeography of living mammals in the Ryukyu Islands.Crossref | GoogleScholarGoogle Scholar |
Nakano, T. (2012). A new species of Orobdella (Hirudinida, Arhynchobdellida, Gastrostomobdellidae) and redescription of O. kawakatsuorum from Hokkaido, Japan with the phylogenetic position of the new species. ZooKeys 169, 9–30.
| A new species of Orobdella (Hirudinida, Arhynchobdellida, Gastrostomobdellidae) and redescription of O. kawakatsuorum from Hokkaido, Japan with the phylogenetic position of the new species.Crossref | GoogleScholarGoogle Scholar |
Nakano, T., Ihara, Y., Kumasaki, Y., Baba, Y. G., and Tomikawa, K. (2017). Evaluation of the systematic status of geographical variations in Arcuphantes hibanus (Arachnida: Araneae: Linyphiidae), with descriptions of two new species. Zoological Science 34, 331–344.
| Evaluation of the systematic status of geographical variations in Arcuphantes hibanus (Arachnida: Araneae: Linyphiidae), with descriptions of two new species.Crossref | GoogleScholarGoogle Scholar | 28770680PubMed |
Ota, H. (1998). Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications. Population Ecology 40, 189–204.
| Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., and Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
| Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |
Ramírez, M. J. (2014). The morphology and phylogeny of dionychan spiders (Araneae: Araneomorphae). Bulletin of the American Museum of Natural History 390, 1–374.
| The morphology and phylogeny of dionychan spiders (Araneae: Araneomorphae).Crossref | GoogleScholarGoogle Scholar |
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 |
Roth, V. D. (1993). ‘Spider Genera of North America with Keys to Families and Genera, and a Guide to Literature’, 3rd edn. (American Arachnological Society: Gainesville, SC, USA.)
Seo, B. K. (2016). Seven new species of the genus Cybaeus (Araneae, Cybaeidae) from Korea. Journal of Species Research 5, 571–583.
| Seven new species of the genus Cybaeus (Araneae, Cybaeidae) from Korea.Crossref | GoogleScholarGoogle Scholar |
Seo, B. K. (2017). Three new species and four new records of the families Cybaeidae and Gnaphosidae (Araneae) from Korea. Journal of Species Research 6, 114–124.
| Three new species and four new records of the families Cybaeidae and Gnaphosidae (Araneae) from Korea.Crossref | GoogleScholarGoogle Scholar |
Shimojana, M. (2000). Description of eleven new species of the genus Coelotes (Araneae: Amaurobiidae) from the Ryukyu Islands, Japan. Acta Arachnologica 49, 165–189.
| Description of eleven new species of the genus Coelotes (Araneae: Amaurobiidae) from the Ryukyu Islands, Japan.Crossref | GoogleScholarGoogle Scholar |
Shimojana, M., and Haupt, J. (1998). Taxonomy and natural history of the funnel-web spider genus Macrothele (Araneae: Hexathelidae: Macrothelinae) in the Ryukyu Islands (Japan) and Taiwan. Species Diversity 3, 1–15.
| Taxonomy and natural history of the funnel-web spider genus Macrothele (Araneae: Hexathelidae: Macrothelinae) in the Ryukyu Islands (Japan) and Taiwan.Crossref | GoogleScholarGoogle Scholar |
Tanikawa, A., and Miyashita, T. (2008). A revision of Japanese spiders of the genus Dolomedes (Araneae: Pisauridae) with its phylogeny based on mt-DNA. Acta Arachnologica 57, 19–35.
| A revision of Japanese spiders of the genus Dolomedes (Araneae: Pisauridae) with its phylogeny based on mt-DNA.Crossref | GoogleScholarGoogle Scholar |
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., and Rozen, S. G. (2012). Primer3 – new capabilities and interfaces. Nucleic Acids Research 40, e115.
| Primer3 – new capabilities and interfaces.Crossref | GoogleScholarGoogle Scholar | 22730293PubMed |
Wessel, P., and Smith, W. H. F. (1996). A global, self-consistent, hierarchical, high-resolution shoreline database. Journal of Geophysical Research. Solid Earth 101, 8741–8743.
| A global, self-consistent, hierarchical, high-resolution shoreline database.Crossref | GoogleScholarGoogle Scholar |
Xu, X., Liu, F., Chen, J., Ono, H., Agnarsson, I., Li, D., and Kuntner, M. (2016). Pre-Pleistocene geological events shaping diversification and distribution of primitively segmented spiders on East Asian margins. Journal of Biogeography 43, 1004–1019.
| Pre-Pleistocene geological events shaping diversification and distribution of primitively segmented spiders on East Asian margins.Crossref | GoogleScholarGoogle Scholar |
Xu, X., Ono, H., Kuntner, M., Liu, F., and Li, D. (2019). A taxonomic monograph of the liphistiid spider genus Heptathela, endemic to Japanese islands. ZooKeys 888, 1–50.
| A taxonomic monograph of the liphistiid spider genus Heptathela, endemic to Japanese islands.Crossref | GoogleScholarGoogle Scholar | 31754317PubMed |