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Type: Article
Published: 2021-08-24
Page range: 71-101
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Molecular phylogeny of pimoid spiders and the limits of Linyphiidae, with a reassessment of male palpal homologies (Araneae, Pimoidae)

Department of Biological Sciences, The George Washington University, Washington, D.C. 20052, USA.
Department of Biological Sciences, The George Washington University, Washington, D.C. 20052, USA.
Department of Biological Sciences, The George Washington University, Washington, D.C. 20052, USA.
Department of Natural History, University Museum of Bergen, University of Bergen, P.O. Box 7800, 5020 Bergen, Norway.
Araneae Systematics Taxonomy Morphology Biogeography Molecular Dating Araneoidea

Abstract

We address the phylogenetic relationships of pimoid spiders (Pimoidae) using a standard target-gene approach with an extensive taxonomic sample, which includes representatives of the four currently recognized pimoid genera, 26 linyphiid genera, a sample of Physoglenidae, Cyatholipidae and one Tetragnathidae species. We test the monophyly of Pimoidae and Linyphiidae and explore the biogeographic history of the group. Nanoa Hormiga, Buckle and Scharff, 2005 and Pimoa Chamberlin & Ivie, 1943 form a clade which is the sister group of a lineage that includes all Linyphiidae, Weintrauboa Hormiga, 2003 and Putaoa Hormiga and Tu, 2008. Weintrauboa, Putaoa, Pecado and Stemonyphantes form a clade (Stemonyphantinae) sister to all remaining linyphiids. We use the resulting optimal molecular phylogenetic tree to assess hypotheses on the male palp sclerite homologies of pimoids and linyphiids. Pimoidae is redelimited to only include Pimoa and Nanoa. We formalize the transfer from Pimoidae of the genera Weintrauboa and Putaoa to Linyphiidae, re-circumscribe the linyphiid subfamily Stemonyphantinae, and offer revised morphological diagnoses for Pimoidae and Linyphiidae.

 

References

  1. Agarwal, I., Bauer, A.M., Jackman, T.R. & Karanth, K.P. (2014) Insights into Himalayan biogeography from geckos: a molecular phylogeny of Cyrtodactylus (Squamata: Gekkonidae). Molecular Phylogenetics and Evolution, 80, 145–155. https://doi.org/10.1016/j.ympev.2014.07.018
    Ali, J.R. & Aitchison, J.C. (2008) Gondwana to Asia: Plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166–35 Ma). Earth Science Review, 88, 145–166. https://doi.org/10.1016/j.earscirev.2008.01.007
    Arnedo, M., Scharff, N. & Hormiga, G. (2009) Higher-level phylogenetics of linyphiid spiders (Araneae, Linyphiidae) based on morphological and molecular evidence. Cladistics, 25 (3), 231–262. https://doi.org/10.1111/j.1096-0031.2009.00249.x
    Blackwall, J. (1859) Descriptions of newly discovered spiders captured by James Yate Johnson Esq., in the island of Madeira. Annals and Magazine of Natural History, Series 3, 4 (22), 255–267. https://doi.org/10.1080/00222935908697122
    Blauvelt, H.H. (1936) The Comparative Morphology of the Secondary Sexual Organs of Linyphia and Some Related Genera, Including a Revision of the Group. Festschrift fur Professor Dr. Strand, 2, 81–171.
    Capella-Gutiérrez, S, Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25 (15), 1972–1973. https://doi.org/10.1093/bioinformatics/btp348
    Clift, P.D., Hodges, K.V., Heslop, D., Hannigan, R., van Long, H. & Calves, G. ( 2008) Correlation of Himalayan exhumation rates and Asian monsoon intensity. Nature Geoscience, 1, 875–880. https://doi.org/10.1038/ngeo351
    Coddington, J.A. (1990) Ontogeny and Homology in the Male Palpus of Orb-Weaving Spiders and Their Relatives, with Comments on Phylogeny (Araneoclada: Araneoidea, Deinopoidea). Smithsonian Contributions to Zoology, 496, 1–52. https://doi.org/10.5479/si.00810282.496
    Dimitrov, D., Benavides, L.R., Arnedo, M.A., Giribet, G., Griswold, C.E., Scharff, N. & Hormiga, G. (2017) Rounding up the usual suspects: a standard target-gene approach for resolving the interfamilial phylogenetic relationships of ecribellate orb-weaving spiders with a new family-rank classification (Araneae, Araneoidea). Cladistics, 33 (3), 221–250. https://doi.org/10.1111/cla.12165
    Dimitrov, D., Lopardo, L., Giribet, G., Arnedo, M.A., Álvarez-Padilla, F. & Hormiga, G. (2012) Tangled in a sparse spider web: single origin of orb weavers and their spinning work unravelled by denser taxonomic sampling. Proceedings of the Royal Society B, 279 (1732), 1341–1350. https://doi.org/10.1098/rspb.2011.2011
    Farris, J.S. (1976) Phylogenetic classification of fossils with recent species. Systematic Zoology 25, 271–282. https://doi.org/10.2307/2412495
    Fernández, R., Kallal, R.J., Dimitrov, D., Ballesteros, J.A., Arnedo, M.A., Giribet, G. & Hormiga, G. (2018) Phylogenomics, Diversification Dynamics, and Comparative Transcriptomics across the Spider Tree of Life. Current Biology, 28 (9), 1489–1497. https://doi.org/10.1016/j.cub.2018.03.064
    Forster, R.R., Platnick, N.I. & Coddington, J. (1990) A proposal and review of the spider family Synotaxidae (Araneae, Araneoidea), with notes on theridiid interrelationships. Bulletin of the American Museum of Natural History, 193, 1–116.
    Frick, H. & Scharff, N. (2013) Phantoms of Gondwana?—phylogeny of the spider subfamily Mynogleninae (Araneae: Linyphiidae). Cladistics, 30 (1), 67–106. https://doi.org/10.1111/cla.12025
    Gavish-Regev, E., Hormiga, G. & Scharff, N. (2013) Pedipalp sclerite homologies and phylogenetic placement of the spider genus Stemonyphantes (Linyphiidae, Araneae) and its implications for linyphiid phylogeny. Invertebrate Systematics, 27 (1), 38–52. https://doi.org/10.1071/IS12014
    Griswold, C.E. (2001) A monograph of the living world genera and Afrotropical species of cyatholipid spiders (Araneae, Orbiculariae, Araneoidea, Cyatholipidae). Memoirs of the California Academy of Sciences, 26, 1–251.
    Griswold, C.E., Coddington, J.A., Hormiga, G. & Scharff, N. (1998) Phylogeny of the orb-web building spiders (Araneae, Orbiculariae: Deinopoidea, Araneoidea). Zoological Journal of The Linnean Society, 123, 1–99. https://doi.org/10.1111/j.1096-3642.1998.tb01290.x
    Guindon, S., Dufayard, J., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321. https://doi.org/10.1093/sysbio/syq010
    Hoang, D.T., Chernomor, O., von Haeseler, A. & Minh, B.-Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518–522. https://doi.org/10.1093/molbev/msx281
    Holt, B.G., Lessard, J.-P., Borregaard, M. K., Fritz, S.A., Araújo, M.B., Dimitrov, D., Fabre, P.-H., Graham, C.H., Graves, G.R., Jønsson, K.A., Nogués-Bravo, D., Wang, Z., Whittaker, R.J., Fjeldså, J. & Rahbek C. (2013) An Update of Wallace’s Zoogeographic Regions of the World. Science, 339, 74–78. https://doi.org/10.1126/science.1228282
    Hormiga, G. (1993) Implications of the phylogeny of Pimoidae for the systematics of linyphiid spiders (Araneae, Araneoidea, Linyphiidae). Memoirs of the Queensland Museum, 33 (2), 533–542.
    Hormiga, G. (1994a) A revision and cladistic analysis of the spider family Pimoidae (Araneae: Araneoidea). Smithsonian Contributions to Zoology, 549, 1–105. https://doi.org/10.5479/si.00810282.549
    Hormiga, G. (1994b) Cladistics and the comparative morphology of linyphiid spiders and their relatives (Araneae, Araneoidea, Linyphiidae). Zoological Journal of the Linnean Society, 111, 1–71. https://doi.org/10.1111/j.1096-3642.1994.tb01491.x
    Hormiga, G. (2003) Weintrauboa, a new genus of pimoid spiders from Japan and adjacent islands, with comments on the monophyly and diagnosis of the family Pimoidae and the genus Pimoa (Araneoidea, Araneae). Zoological Journal of the Linnean Society, 139, 261–281. https://doi.org/10.1046/j.1096-3642.2003.00072.x
    Hormiga, G. (2008) On the spider genus Weintrauboa (Araneae, Pimoidae), with a description of a new species from China and comments on its phylogenetic relationships. Zootaxa, 1814 (1), 1–20. https://doi.org/10.11646/zootaxa.1814.1.1
    Hormiga, G. & Scharff, N. (2005) Monophyly and phylogenetic placement of the spider genus Labulla Simon, 1884 (Araneae, Linyphiidae) and description of the new genus Pecado. Zoological Journal of the Linnean Society, 143, 359–404. https://doi.org/10.1111/j.1096-3642.2005.00147.x
    Hormiga, G. & Tu, L. (2008) On Putaoa, a new genus of the spider Family Pimoidae (Araneae) from China, with a cladistic test of its monophyly and phylogenetic placement. Zootaxa, 1792 (1), 1–21. https://doi.org/10.11646/zootaxa.1792.1.1
    Hormiga, G., Buckle, D.J. & Scharff, N. (2005) Nanoa, an enigmatic new genus of pimoid spiders from western North America (Pimoidae, Araneae). Zoological Journal of the Linnean Society, 145 (2), 249–262. https://doi.org/10.1111/j.1096-3642.2005.00192.x
    Kallal, R.J., Kulkarni, S.K., Dimitrov, Benavides, L.R., Arnedo, M.A., Giribet, G. & Hormiga, G. (2021) Converging on the orb: denser taxon sampling elucidates spider phylogeny and new analytical methods support repeated evolution of the orb web. Cladistics, 37 (3), 298–316. https://doi.org/10.1111/cla.12439
    Kalyaanamoorthy, S., Minh, B.-Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
    Klaus, S., Schubart, C.D., Streit, B. & Pfenninger, M. (2010) When Indian crabs were not yet Asian—biogeographic evidence for Eocene proximity of India and Southeast Asia. BMC Evolutionary Biology, 10, 287. https://doi.org/10.1186/1471-2148-10-287
    Kulkarni, S., Wood, H., Lloyd, M. & Hormiga, G. (2020) Spider-specific probe set for ultraconserved elements offers new perspectives on the evolutionary history of spiders (Arachnida, Araneae). Molecular Ecology Resources, 20, 185–203. https://doi.org/10.1111/1755-0998.13099
    Kulkarni, S.K., Kallal, R.J., Wood, H., Dimitrov, D., Giribet, G. & Hormiga, G. (2021) Interrogating genomic-scale data to resolve recalcitrant nodes in the Spider Tree of Life. Molecular Biology and Evolution, 38 (3), 891–903. https://doi.org/10.1093/molbev/msaa251
    Lavin, M. & Luckow, M. (1993) Origins and relationships of tropical North America in the context of the boreotropics hypothesis. American Journal of Botany, 80, 1–14. https://doi.org/10.1002/j.1537-2197.1993.tb13761.x
    Maddison, W.P. & Maddison, D.R. (2018) Mesquite: a modular system for evolutionary analysis. Version 3.61. Available from http://mesquiteproject.org (accessed 8 June 2021)
    Magalhaes, I.L.F., Azevedo, G.H.F., Michalik, P. & Ramírez, M.J. (2020) The fossil record of spiders revisited: implications for calibrating trees and evidence for a major faunal turnover since the Mesozoic. Biological Reviews, 95, 184–217. https://doi.org/10.1111/brv.12559
    Mammola, S., Hormiga, G., Arnedo, M.A. & Isaia, M. (2016) Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae: Pimoidae). Invertebrate Systematics, 30 (6), 566–587. https://doi.org/10.1071/IS16017
    Mammola, S., Hormiga, G. & Isaia, M. (2017) Species conservation profile of the stenoendemic cave spider Pimoa delphinica (Araneae, Pimoidae) from the Varaita valley (NW-Italy). Biodiversity data journal, 5, e11509. https://doi.org/10.3897/BDJ.5.e11509
    Matzke, N. (2013) BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R scripts. R package. Version 0.2.1. published 27 July 2013. Available from: http://phylo.wikidot.com/biogeobears (accessed 26 July 2021)
    Merrett, P. (1963) The palpus of male spiders of the family Linyphiidae. Proceedings of the Zoological Society of London, 140 (3), 347–467. https://doi.org/10.1111/j.1469-7998.1963.tb01867.x
    Metcalfe, I. (2013) Gondwana dispersion and Asian accretion: tectonic and palaeogeographic evolution of eastern Tethys. Journal of Asian Earth Sciences, 66, 1–33. https://doi.org/10.1016/j.jseaes.2012.12.020
    Michalik, P. & Hormiga, G. (2010) Ultrastructure of the spermatozoa in the spider genus Pimoa—new evidencefor the monophyly of Pimoidae plus Linyphiidae (Arachnida: Araneae). American Museum Novitates, 3682, 1–17. https://doi.org/10.1206/680.1
    Miller, J.A. & Hormiga, G. (2004) Clade stability and the addition of data—a case study from erigonine spiders (Araneae: Linyphiidae, Erigoninae). Cladistics, 20, 385–442. https://doi.org/10.1111/j.1096-0031.2004.00033.x
    Millidge, A.F. (1977) The conformation of the male palpal organs of Linyphiid spiders and its application to the taxonomic and phylogenetic analysis of the family (Araneae: Linyphiidae). Bulletin of the British Arachnological Society, 4, 1–60.
    Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
    Penney, D. & Selden, P.A. (2002) The oldest linyphiid spider, in Lower Cretaceous Lebanese amber (Araneae, Linyphiidae, Linyphiinae). Journal of Arachnology, 30, 487–493. https://doi.org/10.1636/0161-8202(2002)030[0487:TOLSIL]2.0.CO;2
    Ranwez, V., Harispe, S., Delsuc, F. & Douzery, E.J.P. (2011) MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS ONE, 6, e22594. https://doi.org/10.1371/journal.pone.0022594
    Ree, R.H. & Sanmartín, I. (2018) Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. Journal of Biogeography, 45 (4), 741–749. https://doi.org/10.1111/jbi.13173
    Ree, R.H. & Smith, S.A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4–14. https://doi.org/10.1080/10635150701883881
    Saaristo, M.I. (1977) Secondary genital organs in the taxonomy of Lepthyphantinae (Araneae, Linyphiidae). Reports from the Department of Zoology, University of Turku, 5, 1–16.
    Smith, S.A. & O’Meara, B.C. (2012) treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics, 28, 2689–2690. https://doi.org/10.1093/bioinformatics/bts492
    Thaler, K. (1976) Two remarkable relict arachnids from northern Italy: Sabacon simoni Dresco (Opiliones: Ischyropsalididae), Louisfagea rupicola (Simon) (Araneae: Tetragnathidae). Bulletin of the British Arachnological Society, 3 (8), 205–210.
    Tietze, D.T., Packert, M., Martens, J., Lehmann, H. & Sun, Y.-H. (2013) Complete phylogeny and historical biogeography of true rosefinches (Aves: Carpodacus). Zoological Journal of the Linnaean Society, 169, 215–234. https://doi.org/10.1111/zoj.12057
    Tiffney, B. (1985a) The Eocene North Atlantic Land Bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. Journal of the Arnold Arboretum, 66, 243–273. https://doi.org/10.5962/bhl.part.13183
    Tiffney, B.H. (1985b) Perspectives on the origin of the floristic similarity between Eastern Asia and Eastern North America. Journal of the Arnold Arboretum, 66, 73–94. https://doi.org/10.5962/bhl.part.13179
    To, T., Jung, M., Lycett, S. & Gascuel, O. (2016) Fast dating using least-squares criteria and algorithms. Systematic Biology, 65, 82–97. https://doi.org/10.1093/sysbio/syv068
    Van Helsdingen, P.J. (1968) Comparative notes on the species of the Holartic genus Stemonyphantes Menge (Araneida, Linyphiidae). Zoologische Mededelingen, 43, 117–139.
    Wang, F., Ballesteros, J.A., Hormiga, G., Chesters, D., Zhan, Y., Sun, N., Zhu, C., Chen, W. & Tu, L. (2015) Resolving the phylogeny of a speciose spider group, the family Linyphiidae (Araneae). Molecular phylogenetics and evolution, 91, 135–149. https://doi.org/10.1016/j.ympev.2015.05.005
    Wheeler, W.C., Coddington, J.A., Crowley, L.M., Dimitrov, D., Goloboff, P.A., Griswold, C.E., Hormiga, G., Prendini, L., Ramírez, M.J., Sierwald, P., Almeida-Silva, L., Alvarez-Padilla, F., Arnedo, M.A., Benavides Silva, L.R., Benjamin, S.P., Bond, J.E., Grismado, C.J., Hasan, E., Hedin, M., Izquierdo, M.A., Labarque, F.M., Ledford, J., Lopardo, L., Maddison, W.P., Miller, J.A., Piacentini, L.N., Platnick, N.I., Polotow, D., Silva-Dávila, D., Scharff, N., Szűts, T., Ubick, D., Vink, C.J., Wood, H.M. & Zhang, J. (2017) The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling. Cladistics, 33 (6), 574–616. https://doi.org/10.1111/cla.12182
    WSC (2021). World Spider Catalog version 22.0. Natural History Museum Bern. Available at http://wsc.nmbe.ch (accessed 6 July 2021) https://doi.org/10.24436/2.
    Wunderlich, J. (1978) Die Gattungen Stemonyphantes Menge 1866 und Narcissius Jermolajew 1930, mit zwei Neubeschreibungen (Arachnida: Araneae: Linyphiidae). Senckenbergiana Biologica, 59, 125–132.
    Wunderlich, J. (1986) Spinnenfauna gestern und heute: Fossile Spinnen in Bernstein und ihre heute lebenden Verwandten. Quelle & Meyer, Wiesbaden, 283 pp.
    Wunderlich, J. (2004) Descriptions of the first fossil spiders (Araneae) of the family Pimoidae in Baltic amber. Beiträge zur Araneologie, 3, 1279– 1297.
    Yu, Y., Blair, C. & He, X.J. (2020) RASP 4: ancestral state reconstruction Tool for multiple genes and characters. Molecular Biology Evolution, 37, 604–606 https://doi.org/10.1093/molbev/msz257
    Zhang, X.Q., Lan, T.Q., Nie, L. & Li, S.Q. (2020) Eight new species of the spider genus Pimoa (Araneae, Pimoidae) from Tibet, China. ZooKeys, 940, 79–104. https://doi.org/10.3897/zookeys.940.49793
    Zhao, Z., Shao, L., Li, F., Zhang, X. & Li, S. (2020) Tectonic evolution of the Tethyan region created the Eurasian extratropical biodiversity hotspots: tracing Pireneitega spiders’ diversification history. Ecography, 43 (9), 1400–1411. https://doi.org/10.1111/ecog.05044