The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling

Ward C. Wheeler, Jonathan A. Coddington, Louise M. Crowley, Dimitar Dimitrov, Pablo A. Goloboff, Charles E. Griswold, Gustavo Hormiga, Lorenzo Prendini, Martín J. Ramírez, Petra Sierwald, Lina Almeida-Silva, Fernando Alvarez-Padilla, Miquel A. Arnedo, Ligia R. Benavides Silva, Suresh P. Benjamin, Jason E. Bond, Cristian J. Grismado, Emile Hasan, Marshal Hedin, Matías A. IzquierdoFacundo M. Labarque, Joel Ledford, Lara Lopardo, Wayne P. Maddison, Jeremy A. Miller, Luis N. Piacentini, Norman I. Platnick, Daniele Polotow, Diana Fernanda Silva Davila, Nikolaj Scharff, Tamás Szűts, Darrell Ubick, Cor J. Vink, Hannah M. Wood, Junxia Zhang

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184 Scopus citations

Abstract

We present a phylogenetic analysis of spiders using a dataset of 932 spider species, representing 115 families (only the family Synaphridae is unrepresented), 700 known genera, and additional representatives of 26 unidentified or undescribed genera. Eleven genera of the orders Amblypygi, Palpigradi, Schizomida and Uropygi are included as outgroups. The dataset includes six markers from the mitochondrial (12S, 16S, COI) and nuclear (histone H3, 18S, 28S) genomes, and was analysed by multiple methods, including constrained analyses using a highly supported backbone tree from transcriptomic data. We recover most of the higher-level structure of the spider tree with good support, including Mesothelae, Opisthothelae, Mygalomorphae and Araneomorphae. Several of our analyses recover Hypochilidae and Filistatidae as sister groups, as suggested by previous transcriptomic analyses. The Synspermiata are robustly supported, and the families Trogloraptoridae and Caponiidae are found as sister to the Dysderoidea. Our results support the Lost Tracheae clade, including Pholcidae, Tetrablemmidae, Diguetidae, Plectreuridae and the family Pacullidae (restored status) separate from Tetrablemmidae. The Scytodoidea include Ochyroceratidae along with Sicariidae, Scytodidae, Drymusidae and Periegopidae; our results are inconclusive about the separation of these last two families. We did not recover monophyletic Austrochiloidea and Leptonetidae, but our data suggest that both groups are more closely related to the Cylindrical Gland Spigot clade rather than to Synspermiata. Palpimanoidea is not recovered by our analyses, but also not strongly contradicted. We find support for Entelegynae and Oecobioidea (Oecobiidae plus Hersiliidae), and ambiguous placement of cribellate orb-weavers, compatible with their non-monophyly. Nicodamoidea (Nicodamidae plus Megadictynidae) and Araneoidea composition and relationships are consistent with recent analyses. We did not obtain resolution for the titanoecoids (Titanoecidae and Phyxelididae), but the Retrolateral Tibial Apophysis clade is well supported. Penestomidae, and probably Homalonychidae, are part of Zodarioidea, although the latter family was set apart by recent transcriptomic analyses. Our data support a large group that we call the marronoid clade (including the families Amaurobiidae, Desidae, Dictynidae, Hahniidae, Stiphidiidae, Agelenidae and Toxopidae). The circumscription of most marronoid families is redefined here. Amaurobiidae include the Amaurobiinae and provisionally Macrobuninae. We transfer Malenellinae (Malenella, from Anyphaenidae), Chummidae (Chumma) (new syn.) and Tasmarubriinae (Tasmarubrius, Tasmabrochus and Teeatta, from Amphinectidae) to Macrobuninae. Cybaeidae are redefined to include Calymmaria, Cryphoeca, Ethobuella and Willisius (transferred from Hahniidae), and Blabomma and Yorima (transferred from Dictynidae). Cycloctenidae are redefined to include Orepukia (transferred from Agelenidae) and Pakeha and Paravoca (transferred from Amaurobiidae). Desidae are redefined to include five subfamilies: Amphinectinae, with Amphinecta, Mamoea, Maniho, Paramamoea and Rangitata (transferred from Amphinectidae); Ischaleinae, with Bakala and Manjala (transferred from Amaurobiidae) and Ischalea (transferred from Stiphidiidae); Metaltellinae, with Austmusia, Buyina, Calacadia, Cunnawarra, Jalkaraburra, Keera, Magua, Metaltella, Penaoola and Quemusia; Porteriinae (new rank), with Baiami, Cambridgea, Corasoides and Nanocambridgea (transferred from Stiphidiidae); and Desinae, with Desis, and provisionally Poaka (transferred from Amaurobiidae) and Barahna (transferred from Stiphidiidae). Argyroneta is transferred from Cybaeidae to Dictynidae. Cicurina is transferred from Dictynidae to Hahniidae. The genera Neoramia (from Agelenidae) and Aorangia, Marplesia and Neolana (from Amphinectidae) are transferred to Stiphidiidae. The family Toxopidae (restored status) includes two subfamilies: Myroinae, with Gasparia, Gohia, Hulua, Neomyro, Myro, Ommatauxesis and Otagoa (transferred from Desidae); and Toxopinae, with Midgee and Jamara, formerly Midgeeinae, new syn. (transferred from Amaurobiidae) and Hapona, Laestrygones, Lamina, Toxops and Toxopsoides (transferred from Desidae). We obtain a monophyletic Oval Calamistrum clade and Dionycha; Sparassidae, however, are not dionychans, but probably the sister group of those two clades. The composition of the Oval Calamistrum clade is confirmed (including Zoropsidae, Udubidae, Ctenidae, Oxyopidae, Senoculidae, Pisauridae, Trechaleidae, Lycosidae, Psechridae and Thomisidae), affirming previous findings on the uncertain relationships of the “ctenids” Ancylometes and Cupiennius, although a core group of Ctenidae are well supported. Our data were ambiguous as to the monophyly of Oxyopidae. In Dionycha, we found a first split of core Prodidomidae, excluding the Australian Molycriinae, which fall distantly from core prodidomids, among gnaphosoids. The rest of the dionychans form two main groups, Dionycha part A and part B. The former includes much of the Oblique Median Tapetum clade (Trochanteriidae, Gnaphosidae, Gallieniellidae, Phrurolithidae, Trachelidae, Gnaphosidae, Ammoxenidae, Lamponidae and the Molycriinae), and also Anyphaenidae and Clubionidae. Orthobula is transferred from Phrurolithidae to Trachelidae. Our data did not allow for complete resolution for the gnaphosoid families. Dionycha part B includes the families Salticidae, Eutichuridae, Miturgidae, Philodromidae, Viridasiidae, Selenopidae, Corinnidae and Xenoctenidae (new fam., including Xenoctenus, Paravulsor and Odo, transferred from Miturgidae, as well as Incasoctenus from Ctenidae). We confirm the inclusion of Zora (formerly Zoridae) within Miturgidae.

Original languageEnglish
Pages (from-to)574-616
Number of pages43
JournalCladistics
Volume33
Issue number6
DOIs
StatePublished - Dec 2017
Externally publishedYes

Bibliographical note

Funding Information:
C. E. Griswold (CEG) and the CAS Arachnology Lab (L. Almeida-Silva, F. Álvarez-Padilla, J. Ledford, D. Silva-Davila, D. Polotow, F. Labarque, D. Ubick and H. Wood) acknowledge financial support from the CAS Exline-Frizzell Fund for Arachnological Research and CAS Lindsay Expedition Fund and by The Sch-linger Foundation; D. Polotow is grateful for CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico (PDE programme), D. Polotow and L. Almeida-Silva both acknowledge Bill and Maria Peck Fellowships (CAS); and J. Ledford, D. Silva-Davila, F. Álvarez-Padilla, F. Labarque and L. Almeida-Silva acknowledge Schlinger Chair of Arachnology Postdoctoral Fellowships from CAS. T. Szu}ts’ participation was funded by a Marie Curie Intra European Fellowships (Life Sciences Panel, No. 025850) and he acknowledges support from the OTKA/NKFI 106241. Aspects of this research were supported by NSF grants: DEB-0072713 (to CEG and B. Fisher), DEB-9296271 (to CEG), DEB-0613775 (to NIP, CEG, GH, MJR) and BSI-0103795 (to Jablonski and Fritsch, P.I.s). Participation by undergraduate students (Robin Carlson, Joel Ledford, Hillary Guttman, Nibia Soto-Rolón, Christopher Vo, Vanessa Knutson, Jasper Bash, Erika Garcia and Rachel Gibbs) in the CAS Arachnology lab was made possible by NSF BIR-9531307 (to R. Mooi, T. Gosliner and D. Kavanaugh, P.I.s). CEG also thanks Sarah Weigold and Meghan Culpepper for documenting morphology of selected taxa. M. J. Ramírez (MJR) and the MACN lab (C. Grismado, M. Izquierdo, F. Labarque, L. Piacentini) acknowledge financial support from CONICET and grants from FONCyT PICT 2011-1007, PICT-2007-01393, PICT 2003-14092, CONICET PIP 6502, PIP 2008-03209 and PEI 6558.

Funding Information:
Fieldwork was made possible thanks to the support of Andrés A. Ojanguren-Affilastro, Luis Compagnucci, Gonzalo Rubio and Ana Quaglino (Argentina); Barbara Baehr, Lisa Boutin, Mark S. Harvey, Robert Raven and Michael Rix (Australia); Valerio Vignoli (Benin); Joseph Koh and Natalia Chousou-Polydouri (Brunei Darussalem); Elizabeth Arias, Juan Enrique Barriga Tuñón, Camilo I. Mattoni, Peter Michalik and Jose A. Ochoa (Chile); Brian D. Farrell, Kelvin Guer-rero, Jeremy Huff and Erich S. Volschenk (Dominican Republic); Jeremy Huff (French Guiana); Jeremy Huff and Valerio Vignoli (Guinea Bissau and Senegal); Alexander Gromov, Alex and Elena Kreuzberg (Kazakhstan and Uzbekistan); Oscar Francke, Andrew Gluesenkamp, Edmundo González-Santillán, Randy Mercurio, Hector Montaño, Ricardo Paredes, Javier Ponce-Saavedra, Charles Savvas and Peter Sprouse (Mexico); Da Aye Aye Cho, Dong Lin, U Kin Mawng Zaw, U Tin Mya Soe and Joe Slowinski (Myanmar); Tharina and Chris Bird, Quinton and Nicole Martins and Elizabeth Scott (Namibia); Ray Forster, Lyn For-ster and Steven King (New Zealand); Pedro Cardoso (Portugal); Lauren Esposito (Puerto Rico); Ansie Dip-peaar-Schoeman, Ian Engelbrecht, Charles Haddad, Norman Larsen, Robin Lyle, Randy Mercurio, Audrey Ndaba, Elizabeth Scott and Esther van der Westhuizen (South Africa); and Weerachai Nanakorn, Suyanee Vessabutr and Chaweewan Hutacharern (Thailand).

Funding Information:
This work was primarily supported by a grant from the United States National Science Foundation (NSF) (EAR-0228699??Assembling the Tree of Life: Phylogeny of Spiders?) awarded to W. C. Wheeler (P.I.) and J. Coddington (JC), G. Hormiga (GH), L. Prendini (LP) and P. Sierwald (PS) (co-P.I.s). JC acknowledges support from the NMNH Neotropical Lowlands Program, Small Grants Program and Biodiversity of the Guyanas Program, as well as the NSF grants DEB-9712353 (GH, P.I.; JC, co-P.I.) and DBI-0956426 (N. Davies, P.I.; G. Roderick, C. Meyer, JC and T. Orrell, co-P.I.s). Various aspects of this research in the GH Lab at GWU were supported by NSF awards DEB-0328644, DEB-1144492 and DEB-1457300 (to GH and Gonzalo Giribet), by NSF award DEB-0613928 (to N. I. Platnick (P.I.), R. Gillespie, CEG, GH, and PS (co-P.I.s)) and by three NSF REU supplementary grants. GH's stay at the Scharff's lab in the Zoological Museum (University of Copenhagen) was supported by a Villum Kann Rasmussen Fund, VELUX Visiting Professorship. Further support to GH for this project was provided by several awards from GWU. LL acknowledges the Cosmos Club Foundation Program of Grants-in-Aid to Young Scholars and a Weintraub Fellowship from The George Washington University. The participation in this project of F. ?lvarez-Padilla, L. Benavides, S. Benjamin, D. Dimitrov and E. Hasan was made possible in part by support of The George Washington University and the aforementioned NSF awards to GH. F. ?lvarez-Padilla acknowledges support from a scholarship from the Consejo Nacional de Ciencia y Tecnolog?a of Mexico (CONACYT). Aspects of this research conducted in the LP lab at the AMNH, including field collections that contributed material to the project, were supported by NSF awards DEB-0413453 (to LP and W. D. Sissom) and DEB-0640219 (to LP and P. E. Cushing), by a grant from the Richard Lounsbery Foundation (to R. DeSalle, LP and M. E. Siddall), and a Constantine Niarchos Expedition Grant (to LP). PS's fieldwork in South Africa and Myanmar was supported by Field Museum's Marshal Field Fund. C. E. Griswold (CEG) and the CAS Arachnology Lab (L. Almeida-Silva, F. ?lvarez-Padilla, J. Ledford, D. Silva-Davila, D. Polotow, F. Labarque, D. Ubick and H. Wood) acknowledge financial support from the CAS Exline-Frizzell Fund for Arachnological Research and CAS Lindsay Expedition Fund and by The Schlinger Foundation; D. Polotow is grateful for CNPq, Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico (PDE programme), D. Polotow and L. Almeida-Silva both acknowledge Bill and Maria Peck Fellowships (CAS); and J. Ledford, D. Silva-Davila, F. ?lvarez-Padilla, F. Labarque and L. Almeida-Silva acknowledge Schlinger Chair of Arachnology Postdoctoral Fellowships from CAS. T. Sz?ts? participation was funded by a Marie Curie Intra European Fellowships (Life Sciences Panel, No. 025850) and he acknowledges support from the OTKA/NKFI 106241. Aspects of this research were supported by NSF grants: DEB-0072713 (to CEG and B. Fisher), DEB-9296271 (to CEG), DEB-0613775 (to NIP, CEG, GH, MJR) and BSI-0103795 (to Jablonski and Fritsch, P.I.s). Participation by undergraduate students (Robin Carlson, Joel Ledford, Hillary Guttman, Nibia Soto-Rol?n, Christopher Vo, Vanessa Knutson, Jasper Bash, Erika Garcia and Rachel Gibbs) in the CAS Arachnology lab was made possible by NSF BIR-9531307 (to R. Mooi, T. Gosliner and D. Kavanaugh, P.I.s). CEG also thanks Sarah Weigold and Meghan Culpepper for documenting morphology of selected taxa. M. J. Ram?rez (MJR) and the MACN lab (C. Grismado, M. Izquierdo, F. Labarque, L. Piacentini) acknowledge financial support from CONICET and grants from FONCyT PICT 2011-1007, PICT-2007-01393, PICT 2003-14092, CONICET PIP 6502, PIP 2008-03209 and PEI 6558. Aspects of this research in the Scharff lab (NS) at the Zoological Museum, University of Copenhagen, were supported by a grant from the Danish National Science Research Council (SNF21-02-0502). NS acknowledges travel grants for fieldwork in Thailand from DANIDA (Danish development cooperation), as well as from the Carlsberg Foundation (grant no. 0537/60) for fieldwork in Australia. Participation by undergraduate student Jesper Birkedal Schmidt in the NS lab was made possible by the above-mentioned grants. Fieldwork was made possible thanks to the support of Andr?s A. Ojanguren-Affilastro, Luis Compagnucci, Gonzalo Rubio and Ana Quaglino (Argentina); Barbara Baehr, Lisa Boutin, Mark S. Harvey, Robert Raven and Michael Rix (Australia); Valerio Vignoli (Benin); Joseph Koh and Natalia Chousou-Polydouri (Brunei Darussalem); Elizabeth Arias, Juan Enrique Barriga Tu??n, Camilo I. Mattoni, Peter Michalik and Jose A. Ochoa (Chile); Brian D. Farrell, Kelvin Guerrero, Jeremy Huff and Erich S. Volschenk (Dominican Republic); Jeremy Huff (French Guiana); Jeremy Huff and Valerio Vignoli (Guinea Bissau and Senegal); Alexander Gromov, Alex and Elena Kreuzberg (Kazakhstan and Uzbekistan); Oscar Francke, Andrew Gluesenkamp, Edmundo Gonz?lez-Santill?n, Randy Mercurio, Hector Monta?o, Ricardo Paredes, Javier Ponce-Saavedra, Charles Savvas and Peter Sprouse (Mexico); Da Aye Aye Cho, Dong Lin, U Kin Mawng Zaw, U Tin Mya Soe and Joe Slowinski (Myanmar); Tharina and Chris Bird, Quinton and Nicole Martins and Elizabeth Scott (Namibia); Ray Forster, Lyn Forster and Steven King (New Zealand); Pedro Cardoso (Portugal); Lauren Esposito (Puerto Rico); Ansie Dippeaar-Schoeman, Ian Engelbrecht, Charles Haddad, Norman Larsen, Robin Lyle, Randy Mercurio, Audrey Ndaba, Elizabeth Scott and Esther van der Westhuizen (South Africa); and Weerachai Nanakorn, Suyanee Vessabutr and Chaweewan Hutacharern (Thailand). Specimens for this project were provided by Andr?s A. Ojanguren-Affilastro, Ingi Agnarsson, Elizabeth Arias, Barbara Baehr, Domir De Bakker, Jorge Barneche, Jesper Birkedal Schmidt, Marius Burger, Tom?s Cekalovic, Fred Coyle, Sara Crews, Michael Driessen, Ian Engelbrecht, Mike Fitzgerald, Charles Haddad, Mark S. Harvey, Bernhard Huber, Jeremy Huff, Joseph Joh, Matzaj Kuntner, James Lazell, Steven Lew, Camilo Mattoni, Jos? Ochoa, Vladimir Ovtsharenko, Pierre Paquin, Robert Raven, Carles Ribera, Michael Rix, Sergio Rodr?guez Gil, Cristina Scioscia, Carlos Viquez and Peter Weygoldt. DNA sequence data were generated at the AMNH by Rebecca B. Dikow, Torsten Dikow, Jeni Kuszak, Diana Pietri and Dana Price. We thank Bryce McQuillan for providing a photograph of Megadictyna thilenii.

Funding Information:
This work was primarily supported by a grant from the United States National Science Foundation (NSF) (EAR-0228699—’Assembling the Tree of Life: Phylogeny of Spiders’) awarded to W. C. Wheeler (P.I.) and J. Coddington (JC), G. Hormiga (GH), L. Pren-dini (LP) and P. Sierwald (PS) (co-P.I.s). JC acknowledges support from the NMNH Neotropical Lowlands Program, Small Grants Program and Biodiversity of the Guyanas Program, as well as the NSF grants DEB-9712353 (GH, P.I.; JC, co-P.I.) and DBI-0956426 (N. Davies, P.I.; G. Roderick, C. Meyer, JC and T. Orrell, co-P.I.s). Various aspects of this research in the GH Lab at GWU were supported by NSF awards DEB-0328644, DEB-1144492 and DEB-1457300 (to GH and Gonzalo Giribet), by NSF award DEB-0613928 (to N. I. Platnick (P.I.), R. Gillespie, CEG, GH, and PS (co-P.I.s)) and by three NSF REU supplementary grants. GH’s stay at the Scharff’s lab in the Zoological Museum (University of Copenhagen) was supported by a Villum Kann Rasmussen Fund, VELUX Visiting Professorship. Further support to GH for this project was provided by several awards from GWU. LL acknowledges the Cosmos Club Foundation Program of Grants-in-Aid to Young Scholars and a Weintraub Fellowship from The George Washington University. The participation in this project of F. Álvarez-Padilla, L. Benavides, S. Benjamin, D. Dimitrov and E. Hasan was made possible in part by support of The George Washington University and the aforementioned NSF awards to GH. F. Álvarez-Padilla acknowledges support from a scholarship from the Consejo Nacional de Ciencia y Tecnología of Mexico (CONACYT).

Funding Information:
Aspects of this research in the Scharff lab (NS) at the Zoological Museum, University of Copenhagen, were supported by a grant from the Danish National Science Research Council (SNF21-02-0502). NS acknowledges travel grants for fieldwork in Thailand from DANIDA (Danish development cooperation), as well as from the Carlsberg Foundation (grant no. 0537/60) for fieldwork in Australia. Participation by undergraduate student Jesper Birkedal Schmidt in the NS lab was made possible by the above-mentioned grants.

Funding Information:
Aspects of this research conducted in the LP lab at the AMNH, including field collections that contributed material to the project, were supported by NSF awards DEB-0413453 (to LP and W. D. Sissom) and DEB-0640219 (to LP and P. E. Cushing), by a grant from the Richard Lounsbery Foundation (to R. DeSalle, LP and M. E. Siddall), and a Constantine Niarchos Expedition Grant (to LP). PS’s fieldwork in South Africa and Myanmar was supported by Field Museum’s Marshal Field Fund.

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