ZooKeys 440: 57–87, doi: 10.3897/zookeys.440.7891
The deep phylogeny of jumping spiders (Araneae, Salticidae)
Wayne P. Maddison 1,2, Daiqin Li 3,4, Melissa Bodner 2, Junxia Zhang 2, Xin Xu 3, Qingqing Liu 3, Fengxiang Liu 3
1 Beaty Biodiversity Museum and Department of Botany, University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada
2 Department of Zoology, University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada
3 Centre for Behavioural Ecology & Evolution, College of Life Sciences, Hubei University, Wuhan 430062, Hubei, China
4 Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543

Corresponding author: Wayne P. Maddison (wmaddisn@mail.ubc.ca)

Academic editor: Jeremy Miller

received 13 May 2014 | accepted 6 July 2014 | Published 15 September 2014
(C) 2014 Wayne P. Maddison. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
For reference, use of the paginated PDF or printed version of this article is recommended.

Citation: Maddison WP, Li D, Bodner M, Zhang J, Xu X, Liu Q, Liu F (2014) The deep phylogeny of jumping spiders (Araneae, Salticidae). ZooKeys 440: 57–87. doi: 10.3897/zookeys.440.7891

Abstract

In order to resolve better the deep relationships among salticid spiders, we compiled and analyzed a molecular dataset of 169 salticid taxa (and 7 outgroups) and 8 gene regions. This dataset adds many new taxa to previous analyses, especially among the non-salticoid salticids, as well as two new genes – wingless and myosin heavy chain. Both of these genes, and especially the better sampled wingless, confirm many of the relationships indicated by other genes. The cocalodines are placed as sister to lapsiines, in a broader clade with the spartaeines. Cocalodines, lapsiines, and spartaeines are each supported as monophyletic, though the first two have no known morphological synapomorphies. The lyssomanines appear to be non-monophyletic, of three separate groups: (1) Lyssomanes plus Chinoscopus, (2) Onomastus, and (3) the remainder of Old World species. Several previously-inferred relationships continue to be supported: hisponines as sister to the Salticoida, Amycoida as sister to the remaining Salticoida, and Saltafresia as monophyletic. The relationship of Salticus with Philaeus and relatives is now considered well enough corroborated to move the latter into the subfamily Salticinae. A new clade consisting of the Plexippoida + Aelurilloida + Leptorchesteae + Salticinae is recognized. Nungia is found to be an astioid, and Echeclus, Gedea and Diplocanthopoda to be hasariines. The euophryines are corroborated as monophyletic. The agoriines Agorius and Synagelides are salticoids, within the sister group to amycoids, but their further placement is problematical, perhaps because of their nuclear ribosomal genes’ high GC bias, as also seen in the similarly problematic Eupoa.

Keywords

Jumping spiders, Salticidae, phylogeny, systematics

Introduction

Salticid spiders, remarkable for their excellent vision (Land 1969, Blest et al. 1990), include more than 5000 species (Platnick 2014) with a great diversity of body forms and behaviours. While this diversity has long resisted phylogenetic organization, recent molecular studies (Maddison and Hedin 2003, Su et al. 2007, Maddison et al. 2008, Bodner and Maddison 2012, Zhang and Maddison 2013), aided by compilations of morphological taxonomic knowledge (Prószyński 2013) have resolved much of the phylogenetic structure of the family. One of the best-supported clades is the Salticoida, recognized by both morphological and molecular data (Maddison 1996, Maddison and Hedin 2003) and containing about 95% of the known species in the family. Within the Salticoida, large groups such as the Amycoida, Astioida, Marpissoida and Plexippoida are well-corroborated (Maddison and Hedin 2003, Maddison et al. 2008). However, many of the deeper relationships of salticoids have been poorly resolved. Outside the Salticoida are the spartaeines, lyssomanines, and hisponines, showing ancestral features like limited tracheal systems, complex palpi, and the retention of a tarsal claw on the female palp. These non-salticoids (often called “basal salticids”) have been studied phylogenetically (Su et al. 2007), but with limited taxon sampling.

In this work we attempt to resolve more firmly the basic structure of the family by increasing the taxon sampling, especially among non-salticoid salticids, and by using additional genes. Two of the genes, wingless and myosin heavy chain, are new to salticid molecular phylogenetics. By building a dataset that has a greater number of genes among selected species, we hoped to obtain a phylogenetic resolution with stronger confidence.

Methods
Taxon sampling

Taxa included in the analysis are 169 species of salticids and representatives of four dionychan families as outgroups (Table 1, Suppl. material 1). Based on previous phylogenetic work (Maddison and Hedin 2003, Maddison et al. 2008, Bodner and Maddison 2012, Zhang and Maddison 2013, in press), about 70 species of salticids from the major clade Salticoida were selected because they would represent most known major lineages, and because several genes are available for each (Table 1, Suppl. material 1). In addition, a few salticoids were added because their placement was unclear: Agorius, Diplocanthopoda, Echeclus, Gedea, Nungia, Phaulostylus, and Synagelides.

Table 1.

Specimens and sequences used in phylogenetic analyses, with GenBank numbers indicated. * marks previously published sequences. Specimen localities given in Suppl. material 1.

Reference 28s 18s wingless myosin HC actin 5c histone 3 CO1 16sND1
Outgroups
Anyphaenidae: Hibana sp. s318 AY297295* KM033091 KM032961 KM032929 AY297422* AY297295 / AY297358*
Gnaphosidae: Cesonia sp. s319 AY297293; EF201663* KM032996 EU522700* DQ665720* AY297420* AY296711 / AY297356*
Miturgidae: Cheiracanthium sp. s321 AY297294; EF201664* KM032997 KM032928 AY297421* AY296712 / AY297357*
Oxyopidae: Oxyopes birmanicus Thorell, 1887 Su et al. 2007 EF419032 / EF419065* EF418998* EF419126* EF419097* EF418969 / EF419150*
Philodromidae: Philodromus alascensis Keyserling, 1884 GR011 KM033130 KM033092 KM032998 KM032962
Thomisidae: Misumenops nepenthicola (Pocock, 1898) Su et al. 2007 EF419029 / EF419062* EF418996* EF419123* EF419094* EF418967 / EF419148*
Thomisidae: Xysticus sp. s316 AY297296; EF201665* KM033093 EU522701* DQ665704* AY297296* AY296714 / AY297359*
Lyssomanines
Asemonea sichuanensis Song & Chai, 1992 SC-03-0055 EF418986* EF419082*
Asemonea sichuanensis Song & Chai, 1992 MRB084 KM033131 KM032931
Asemonea cf. stella Wanless, 1980 MRB083 JX145767* KM033094 KM032930 JX145686*
Asemonea tenuipes (O. P.-Cambridge, 1869) d186 KM033132 KM033095 KM032999 KM032963 KM032932
Chinoscopus cf. flavus (Peckham, Peckham & Wheeler, 1889) d273 KM033133 KM033096 KM032888
Goleba lyra Maddison & Zhang, 2006 d051 DQ665768* KM033097 KM033000 EU522709* DQ665707* DQ665755*
Lyssomanes amazonicus Peckham & Wheeler, 1889 ECU11-6112 KM033134 KM032889
Lyssomanes antillanus Peckham & Wheeler, 1889 d298 KM033135 KM033001
Lyssomanes cf. benderi Logunov, 2002 ECU11-5402 KM033136 KM032890
Lyssomanes cf. jemineus Peckham & Wheeler, 1889 ECU11-5682 KM033137 KM032891
Lyssomanes longipes (Taczanowski, 1871) MRB086 KM033138 KM032933 KM033208 KM032892
Lyssomanes pauper Mello-Leitão, 1945 d297 KM033139 KM033002
Lyssomanes taczanowskii Galiano, 1980 ECU11-4193 KM033141 KM032894
Lyssomanes tenuis Peckham & Wheeler, 1889 ECU11-4869 KM033142 KM032895
Lyssomanes viridis (Walckenaer, 1837) s160 AY297231* AY297360* AY296652 / AY297297*
Lyssomanes viridis (Walckenaer, 1837) d129 KM033098 KM033003 EU522715* DQ665715*
Lyssomanes sp. [Esmeraldas] d408 KM033140 KM032893
Onomastus nigrimaculatus Zhang & Li, 2005 Su et al. 2007 EF419031 / EF419064* EF418997* EF419125* EF419096* EF418968 / EF419149*
Onomastus sp. [Guangxi] MRB085 JX145768* KM033099 KM033004 KM032964 KM032934 JX145687* JX145910*
Pandisus cf. decorus Wanless, 1980 d303 KM033143 KM033005
Cocalodines
Allococalodes madidus Maddison, 2009 d236 KM033144 KM033006 KM032896
Cocalodes longicornis Wanless, 1982 d291 KM033145 KM033007 KM032935 KM032897
Cocalodes macellus (Thorell, 1878) d230 KM033146 KM033100 KM033008 KM032936 KM033209
Cucudeta gahavisuka Maddison, 2009 d234 KM033147 KM033009 KM032898
Cucudeta zabkai Maddison, 2009 d235 KM033148 KM033010 KM032965 KM032899
Tabuina aff. baiteta Maddison, 2009 d313 KM033149 KM033011
Tabuina rufa Maddison, 2009 d232 KM033151 KM033013 KM032900
Tabuina aff. rufa Maddison, 2009 d312 KM033150 KM033012
Tabuina varirata Maddison, 2009 d233 KM033152 KM033014 KM032901
Yamangalea frewana Maddison, 2009 d231 KM033153 KM033015 KM032902
Spartaeines
Brettus cf. adonis Simon, 1900 SWK12-4323 KM033154
Brettus sp. [Yunnan] LiD-026-053-05 KM033155S KM033101S KM033195S
cf. Phaeacius sp. [Sarawak] SWK12-3728 KM033156
Cocalus murinus Simon, 1899 LiD-013-027-05 EF419019 / EF419053* EF418988* EF419116* EF419084* EF418959 / EF419140*
Cyrba algerina (Lucas, 1846) Su et al. 2007 EF419021 / EF419054* EF418989* EF419086* EF418961 / EF419142*
Cyrba lineata Wanless, 1984 MRB106 JX145792* KM033016 KM032966 KM032937 JX145704*
Cyrba ocellata (Kroneberg, 1875) Su et al. 2007 EF418990* EF419087* EF418962 / EF419143*
Cyrba ocellata (Kroneberg, 1875) MRB104 KM033157
Cyrba sp. [Kenya] Su et al. 2007 EF419023 / EF419056* EF418991* EF419088*
Gelotia cf. bimaculata Thorell, 1890 d250 KM033158 KM033017 KM032938
Gelotia syringopalpis Wanless, 1984 Su et al. 2007 EF419024 / EF419057* EF419118*
Gelotia syringopalpis Wanless, 1984 MRB105 KM033019 KM033212 KM032903
Gelotia sp. [Guangxi] MRB199 KM033018 KM032939 KM033210
Gelotia sp. [Yunnan] LiD002-053-05 KM033102S KM033196S KM033211S
Holcolaetis vellerea Simon, 1910 Su et al. 2007 EF419025 / EF419058* EF418992* EF419119* EF419090* EF418963 / EF419144*
Holcolaetis cf. zuluensis Lawrence, 1937 d036 DQ665770* KM033103 EU522711* DQ665721* DQ665757*
Meleon aff. kenti (Lessert, 1925) d287 KM033159 KM032940
Mintonia mackiei Wanless, 1984 SWK12-4202 KM033161
Mintonia cf. melinauensis Wanless, 1984 d441 KM033160
Mintonia ramipalpis (Thorell, 1890) SWK12-1442 KM033162
Mintonia silvicola Wanless, 1987 d104 KM033020 KM032904
Mintonia silvicola Wanless, 1987 SWK12-1653 KM033163
Mintonia silvicola Wanless, 1987 Su et al. 2007 EF418995* EF419122* EF419093*
Mintonia tauricornis Wanless, 1984 d249 KM033164 KM033021 KM032941 KM032905
Neobrettus tibialis (Prószyński, 1978) LiD-001-055-05 EF419030 / EF419063* EF419124* EF419095*
Neobrettus sp. [Sarawak] SWK12-1040 KM033165
Paracyrba wanlessi Zabka & Kovac, 1996 Su et al. 2007 EF419033 / EF419066* EF418999* EF419098*
Phaeacius lancearius (Thorell, 1895) d111 DQ665775* KM033022 DQ665759*
Phaeacius malayensis Wanless, 1981 Su et al. 2007 EF419034 / EF419067* EF419000* EF419099* EF418970 / EF419151*
Phaeacius sp. [Guangxi] LQ-24-06 KM033166S KM033104S KM033213S KM032906S
Phaeacius sp. [Hainan] Su et al. 2007 EF419035 / EF419068* EF419001* EF418971 / EF419152*
Phaeacius sp. [Sarawak] SWK12-4541 KM033167
Portia africana (Simon, 1886) Su et al. 2007 EF419037 / EF419069* EF419003* EF419128* EF419101*
Portia crassipalpis (Peckham & Peckham, 1907) SWK12-2354 KM033168
Portia fimbriata (Doleschall, 1859) LiD-001-04 EF419038 / EF419070* EF419004* EF419129* EF419102* EF418973 / EF419154*
Portia heteroidea Xie & Yin, 1991 Su et al. 2007 EF419039 / EF419071* EF419005* EF419130* EF419103* EF418974 / EF419155*
Portia jianfeng Song & Zhu, 1998 Su et al. 2007 EF419040 / EF419072* EF419006* EF419104* EF418975 / EF419156*
Portia labiata (Thorell, 1887) S206 AY297232* AY297361* AY296653 / AY297298*
Portia cf. schultzi Karsch, 1878 d131 DQ665776* KM033105 KM033023 KM032967 EU522718* DQ665708*
Portia quei Zabka, 1985 Su et al. 2007 EF419042 / EF419074* EF419008* EF419132* EF419106* EF418977 / EF419158*
Portia taiwanica Zhang & Li, 2005 MRB103 KM033169 KM032942 KM033214 KM032907
Portia sp. [Sichuan] SC-03-0011 EF419043 / EF419075* EF419009* EF419133* EF418978 / EF419159*
Sonoita lightfooti Peckham & Peckham, 1903 d226 KM033170 KM033215
Sonoita aff. lightfooti Peckham & Peckham, 1903 MRB200 JX145791* JX145705* JX145927*
Sparbambus gombakensis Zhang, Woon & Li, 2006 d251 KM033171 KM033024 KM032943
Spartaeus jianfengensis Song & Chai, 1991 Su et al. 2007 EF419045 / EF419076* EF419011* EF419109* EF418980 / EF419161*
Spartaeus platnicki Song, Chen & Gong, 1991 SC-03-069 EF419046 / EF419077* EF419012* EF419135* EF419110* EF418981 / EF419162*
Spartaeus spinimanus (Thorell, 1878) S199 KM033216 KM032908
Spartaeus thailandicus Wanless, 1984 BV-004 EF419047 / EF419078* EF419013* EF419136* EF419111* EF418982 / EF419163*
Spartaeus uplandicus Barrion & Litsinger, 1995 S185/S186 AY297233* AY297363* AY296655*
Spartaeus wildtrackii Wanless, 1987 Su et al. 2007 EF419048 / EF419079* EF419014* EF419137* EF419112* EF418983 / EF419164*
Taraxella sp. [Johor] d246 KM033172 KM032944 KM032909
Taraxella sp. [Pahang] d248 KM033173 KM032945 KM033197
Taraxella sp. [Pahang] LiD-001-003-06 KM033106S KM033217S KM032910S
Yaginumanis wanlessi Zhang & Li, 2005 Su et al. 2007 EF419050 / EF419081* EF419016* EF419139* EF419114* EF418985 / EF419166*
Lapsiines
Galianora bryicola Maddison, 2006 d124 DQ665771* DQ665741* KM033025 EU522706* DQ665717* DQ665758* DQ665727*
Galianora sacha Maddison, 2006 d116 DQ665766* DQ665734* KM033026 KM032968 EU522707* DQ665716* DQ665754*
Lapsias canandea Maddison, 2012 d442 KM033174
Lapsias guamani Maddison, 2012 UBC-SEM AR00191 KM033175 KM033027
Lapsias lorax Maddison, 2012 UBC-SEM AR00194 KM033176 KM033028
Soesiladeepakius lyra Ruiz & Maddison, 2012 GR130 JQ312077 KM033029 JQ312074* JQ312079*
Thrandina bellavista Maddison, 2012 d396 KM033177 KM033030
Thrandina cosanga Maddison, 2012 d395 KM033178
Thrandina parocula Maddison, 2006 d123 DQ665779* KM033107 EU522720* DQ665718* DQ665761* DQ665726*
Thrandina parocula Maddison, 2006 d394 KM033031 KM032969
Eupoa
Eupoa nezha Maddison & Zhang, 2007 d220/MRB102 EF201648* EF201666* KM033032 EF201668* EF201667*
Hisponines
cf. Tomocyrba sp. [Madagascar] d305 KM032881*
Hispo macfarlanei Wanless, 1981 d404 KM032882* KM032970
Hispo sp. [Madagascar] d309 KM032883*
Jerzego cf. alboguttatus Simon, 1903 SWK12-4787 KM032884*
Jerzego corticicola Maddison, 2014 SWK12-2900 KM032885* KM032887*
Massagris contortuplicata Wesolowska & Haddad, 2013 d082 DQ665772* KM033108 KM033033 DQ665705* DQ665722*
Massagris schisma Maddison & Zhang, 2006 d081 DQ665762* KM033109 KM033034 DQ665728*
Tomobella andasibe (Maddison & Zhang, 2006) d127 DQ665780* DQ665752* KM033035 KM033198 DQ665725*
Tomocyrba sp. [Madagascar] d306 KM032886*
Tomomingi sp. [Gabon] MRB243 JX145764* KM033110 KM033036 KM032971 JX145850* JX145684*
Salticoida
Agoriines
Agorius constrictus Simon, 1901 d172 KM032953
Agorius constrictus Simon, 1901 d213 KM033119 KM033072 KM032921
Agorius sp. [Selangor] d299 KM033189 KM033073
Synagelides cf. lushanensis Xie & Yin, 1990 d214 KM033074
Synagelides cf. palpalis Zabka, 1985 MRB050 KM032922
Synagelides cf. palpalis Zabka, 1985 d225 KM033190 KM033226
Amycoids
Cotinusa sp. [Ecuador] MRB024 JX145746* KM033120 KM033075 KM032987 JX145832* JX145671* JX145896*
Hurius vulpinus Simon, 1901 S213 AY297239* AY297368* AY296662 / AY297306*
Hurius cf. vulpinus Simon, 1901 d156 KM033076 EU522712* KM033203
Hypaeus aff. miles Simon, 1900 [Ecuador] d130 EU815499* KM033121 KM033077 KM032988 EU522702* KM032923
Sarinda cutleri (Richman, 1965) MRB193 JX145744* KM033078 KM032954 JX145669* JX145895*
Sitticus floricola palustris (Peckham & Peckham, 1883) d030 DQ665778* KM033122 KM033079 KM032989 KM033204 DQ665760* DQ665729*
Astioids
Arasia mollicoma (L. Koch, 1880) d046 EU815483* EU815532* KM032990 JX145834* KM033205 EU815598* EU815550*
Helpis minitabunda (L. Koch, 1880) d265 KM033123 KM033080 KM032991 KM032955 KM033227
Ligurra latidens (Doleschall, 1859) d175 JX145749* KM033081 JX145835* JX145898*
Ligurra latidens (Doleschall, 1859) LiD-001-027-05 EF418993* EF419120* EF419091*
Mopsus mormon Karsch, 1878 d018 EU815470* EU815529* KM033082 JX145836* KM033206 EU815586*
Myrmarachne sp. [Pahang] d162 EU815507* KM033124 KM033083 KM032992 JX145837* EU815616* EU815565*
Neon reticulatus (Blackwall, 1853) d283 KM033191 KM033125 KM033084 KM032993 KM032956
Nungia epigynalis Zabka, 1985 d221 KM033192 KM032924
Simaetha sp. d027 EU815477* KM033126 KM033085 JX145839* EU815592* EU815546*
Trite pennata Simon, 1885 d035 EU815478* KM033086 KM032957 KM033207 EU815593* EU815547*
Baviines
Bavia aff. aericeps Simon, 1877 [Sabah] d079 EU815490* KM033127 KM032958 EU815603* KM032925
Stagetilus sp. [Selangor] MRB079 KM033193 KM033087 KM032959 KM032926
Marpissoids
Afromarengo sp. [Gabon] MRB262 JX145758* KM033128 KM033088 KM032994 JX145842* JX145682* JX145905*
Dendryphantes hastatus (Clerck, 1757) d043 EF201646* KM033129 KM033089 KM033228 KM032927
Platycryptus californicus (Peckham & Peckham, 1888) d316 KM033194 KM033090 KM032995 KM032960 KM033229
Rhene sp. [Pahang] LiD-001-021-05 EF419044* EF419010* EF419134* EF419108* EF418979 / EF419160*
Tisaniba mulu Zhang & Maddison, 2014 SWK12-1244 KM032876* KM032880*
Saltafresians
Aelurillus cf. ater (Kroneberg, 1875) d140 EU815504* EU815536* KM033037 KM032972 JX145831* KM033199 EU815615* EU815564*
Amphidraus complexus Zhang & Maddison, 2012 JXZ035 KC615380* KM033038 KC616069* KC615640* KC615806*
Athamas cf. whitmeei O. P.-Cambridge, 1877 JXZ345 KC616286* KC615649* KC615822*
Bacelarella pavida Szüts & Jocqué, 2001 d195 EU815511* EU815538* KM033039 KM032973 KM032946 EU815618* EU815569*
Bathippus macrognathus (Thorell, 1881) JXZ372 KC615407* KM033040 KC616305* KC615835*
Bianor maculatus (Keyserling, 1883) d017 EU815469* KM033041 KM033200 EU815585* EU815542*
Bristowia afra Szüts, 2004 JXZ363 KC615409* KC616301*
Bristowia afra Szüts, 2004 MRB230 KM033042 KM033218
Cheliceroides longipalpis Zabka, 1985 d222 KM033111 KM033043 JX145830* KM033219 EU815579*
Cheliceroides cf. longipalpis Zabka, 1985 d415 KM033179
Chinattus parvulus (Banks, 1895) d009 EU815464* EU815525* KM033044 JX145848* KM033201 EU815581*
Chinophrys pengi Zhang & Maddison, 2012 JXZ145 KC615416* KM033045 KC616146* KC615843*
Corythalia locuples (Simon, 1888) JXZ315 KC615390* KM033046 KC616260* KC615645* KC615816*
Cosmophasis umbratica Simon, 1903 Su et al. 2007 EF419020* EF419117* EF419085* EF418960 / EF419141*
Cytaea nimbata (Thorell, 1881) JXZ229 KC615474* KM033047 KC616197* KC615693* KC615899*
Diolenius varicus Gardzińska & Zabka, 2006 JXZ349 KC615480* KM033048 KC616290* KC615695* KC615905*
Diplocanthopoda marina Abraham, 1925 d209 KM033180 KM032947 KM033220 KM032911
Eburneana sp. [Gabon] MRB231 KM033181 KM033049 JX145858* KM033221 KM032912
Echeclus sp. [Selangor] MRB089 KM033182 KM032948 KM033222 KM032913
Euophrys frontalis (Walckenaer, 1802) JXZ137 KC615536* KM033050 KC616139* KC615960*
Evarcha proszynskii Marusik & Logunov, 1998 d096 DQ665765* KM033112 EU522704* DQ665723*
Evarcha proszynskii Marusik & Logunov, 1998 d323 KM033051 KM032974
Freya decorata (C. L. Koch, 1846) d211 EU815521* EU815539* KM032975 EU522705* JX145908*
Gedea cf. tibialis Zabka, 1985 MRB090 KM033183 KM032949 KM033223 KM032914
Habrocestum cf. albimanum Simon, 1901 d132 EU815500* EU815611* EU815562*
Habronattus borealis (Banks, 1895) d207 KM033184 KM033052 KM032976 KM032950 KM033224 KM032915
Hasarius adansoni (Audouin, 1826) d295 KM033113 KM033053 KM032977
Hasarius adansoni (Audouin, 1826) S130/S131/S324 AY297281* AY297409*
Heliophanus cupreus (Walckenaer, 1802) d044 DQ665769* KM033114 EU522710* DQ665710* DQ665756* KM032916
Idastrandia cf. orientalis (Szombathy, 1915) d108 EU815535; EU815496* EU815535* JX145852* EU815608* EU815560*
Langerra aff. longicymbium Song & Chai, 1991 d182 KM033185 KM033054 KM032917
Leptorchestes berolinensis (C. L. Koch, 1846) d086 EU815491* EU815534* KM033055 EU815604* EU815556*
Longarenus brachycephalus Simon, 1903 MRB258 JX145798* KM033056 KM032978 KM032951 JX145707* KM032918
Nannenus sp. [Pahang] d105 EU815493* KM033057 KM032979 JX145853* EU815558*
Naphrys pulex (Hentz, 1846) JXZ081 JX145760* KM033115 KM032980 JX145844* KC615749* JX145907*
Omoedus orbiculatus (Keyserling, 1881) d008 KC615792*
Omoedus orbiculatus (Keyserling, 1881) JXZ136 JX145762* KM033116 KM033058 JX145846* KM033202
Omoedus papuanus Zhang & Maddison, 2012 JXZ286 KC615619* KM033059 KC616234* KC615790* KC616042*
Pellenes peninsularis Emerton, 1925 d057 DQ665774* KM033117 KM033060 JX145864* DQ665712*
Pellenes peninsularis Emerton, 1925 d400 KM032981
Phaulostylus grammicus Simon, 1902 d304 KM033186 KM033061
Philaeus chrysops (Poda, 1761) d025 EU815475* EU815530* KM033062 JX145855* EU815590* EU815545*
Phintella sp. [Gabon] d402 KM033187 KM033063 KM032982
Plexippus paykulli (Audouin, 1826) LiD-001-029-05 EF419002* EF419127*
Plexippus paykulli (Audouin, 1826) MRB016 JX145784* KM033064 EU522713*
Plexippus paykulli (Audouin, 1826) S73 AY297384* AY296674 / AY297317*
Pochyta cf. pannosa Simon, 1903 MRB257 JX145806* KM033065 KM032983 KM032952 JX145715* KM032919
Saitis barbipes (Simon, 1868) JXZ147 KC615589* KM033066 KC616147* KC615767* KC616011*
Salticus scenicus (Clerck, 1757) d003 DQ665777* KM033118 KM033067 KM032984 EU522719* DQ665713* JX145663* AY296707 / AY297352*
Thiania bhamoensis Thorell, 1887 LiD-001-028-05 EF419049 / EF419080* EF419015* EF419138* EF419113* EF418984 / EF419165*
Trydarssus cf. nobilitatus (Nicolet, 1849) MRB270 KM033188 KM033068 KM032985 JX145847* KM033225 KM032920
Tusitala lyrata (Simon, 1903) MRB226 JX145771* KM033069 JX145856* JX145689* JX145912*
Yllenus arenarius Menge, 1868 d013 EU815527* EU815583* EU815541*
Yllenus arenarius Menge, 1868 JXZ173 JX145766* KM033070 KM032986 JX145851*
Zabkattus furcatus Zhang & Maddison, 2012 JXZ218 KC615503* KM033071 KC616190* KC615928*

Our sample targeted especially the non-salticoid salticids, those that lie outside the major clade of familiar salticids (Maddison and Needham 2006). We included most available data from non-salticoid salticids, both new data and data previously published by Su et al. (2007) and others (Maddison and Hedin 2003, Maddison and Needham 2006, Maddison et al. 2007, Bodner and Maddison 2012, Ruiz and Maddison 2012, Zhang and Maddison 2013, Maddison and Piascik, in press). Included for the first time in a molecular phylogeny are the cocalodines (Wanless 1982, Maddison 2009), which are Australasian non-salticoid salticids. Also analyzed for the first time are the lyssomanine genera Chinoscopus and Pandisus, the lapsiine Lapsias, and the spartaeines Brettus, Meleon, Sparbambus, and Taraxella.

Some previously-published data from non-salticoid salticids was either excluded or represented under a different species name here. Excluded are sequences of Hispo cf. frenata, because its limited data made it unstable in the analyses (see Maddison and Piascik 2014), “Portia labiata” from Su et al. (2007), because its identification is in doubt and no voucher specimen is available, and the actin 5C sequence of Tomomingi sp. voucher d243, which we discovered to have been a contaminant from the euophryine Ilargus. The species labeled as Phaeacius yixin by Su et al. (2007) is included here as “Phaeacius sp. [Hainan]”, because the specimen was a juvenile female and thus identified with doubt; by its DNA we suspect it is Phaeacius lancearius. The specimen labeled as Mintonia ramipalpis by Su et al. (2007) is actually a female Mintonia silvicola. This misidentification arose because of an error in male-female matching by Wanless (1984), whose female “Mintonia ramipalpis” is actually the female of Mintonia silvicola. The correct match of male and female Mintonia silvicola is evident by intimate co-collecting in a recent expedition to Sarawak (Maddison and Piascik, unpublished) and in DNA sequence comparison. We have therefore blended data from Su et al.’s female with that from our males to represent Mintonia silvicola.

Some of the species studied appear to be undescribed, or are doubtfully the same as described species. Following the usual convention, the names of some of our specimens includes “cf.” to indicate that they may be the same as the mentioned species, “aff.” to indicate that they are close to, but distinctly different from, the mentioned species. Figures 1–13 give illustrations of some of the undescribed species, in order to facilitate future association of our data with a species name. The species we refer to as “cf. Phaeacius [Sarawak]” (Figs 1, 2) is known from a single female and juvenile from Lambir Hills, Sarawak. It resembles Phaeacius but the legs are shorter, and the epigynum is distinctively different. Phaeacius sp. [Sarawak] (Figs 3, 4) is a fairly typical Phaeacius whose epigynum resembles that of Phaeacius leytensis Wijesinghe, 1991, but with the atria elongated posteriorly. Onomastus sp. [Guangxi] is shown in Fig. 5. Sonoita aff. lightfooti (Fig. 6) has longer grooves for the openings of the epigynum than Sonoita lightfooti, and is distinctive in gene sequences as well. Gelotia sp. [Guangxi] (Fig. 7) has a palp resembling Gelotia syringopalpis, but the tibial apophyses are much shorter. Echeclus sp. [Selangor] (Figs 8, 9) was identified as an Echeclus by the distinctive form of the palp tibia, and the embolus hidden behind a ledge of the tegulum, through which several dark sclerites can be seen (Prószyński 1987). It might equally well have been identified, by the same features, as a Curubis species (Zabka 1988). Indeed, the two genera are likely synonyms. “Echeclus” is used as that is the older name. Taraxella sp. [Johor] (Figs 10, 11) and Taraxella sp. [Pahang] (Figs 12, 13) are typical species of Taraxella. The specimen MRB024 identified as Cotinusa sp. is the same as that named “unidentified thiodinine” by Bodner and Maddison (2012). The Hypaeus specimen (d130) was formerly identified as Acragas sp. (Bodner and Maddison 2012). The specimen d105 labeled as “Nannenus lyriger” by Maddison et al. (2008) is not Nannenus lyriger, but another apparently undescribed species of Nannenus. The data for Cheliceroides longipalpis comes from two specimens, d222 which is clearly Cheliceroides longipalpis, and d415 which may be a different but very closely related species. Notes on the undescribed hisponines are given by Maddison and Piascik (2014), whose data we use.

Figures 1–13.

Specimens of undescribed species. 1, 3, 5, 6 are of epigyna, ventral view; 8, 11, 13 of left palps, ventral view; 7 of the right palp tibia, retrolateral view. Scale bar 0.1 mm. 1–2 Female cf. Phaeacius [Sarawak], voucher SWK12–3728 3–4 Female Phaeacius sp. [Sarawak], voucher SWK12–4541 5 female Onomastus sp. [Guangxi], voucher MRB085 6 Female Sonoita aff. lightfooti, voucher MRB200. 7 male Gelotia sp. [Guangxi], voucher MRB199. The drawing is reversed so as to appear to be the left palpus 8–9 Male Echeclus sp. [Selangor], voucher MRB089 10–11 Male Taraxella sp.[Johor], voucher d246 for the palpus. The photo of the living male may or may not be of the same specimen 12–13 Male Taraxella sp. [Pahang], voucher d248. The photo of the living male may or may not be of the same specimen. Figures 1–13 are copyright ©2014 W.P. Maddison, released under a Creative Commons Attribution (CC-BY) 3.0 license.

Specimens whose voucher ID’s (Table 1, Suppl. material 1) are of the form S###, d###, MRB###, or JXZ###, SWK12-####, or ECU11-####, where # is a digit, are deposited in the Spencer Entomological Collection of the Beaty Biodiversity Museum, University of British Columbia. The remaining vouchers are in the Lee Kong Chian Natural History Museum (formerly Raffles Museum for Biodiversity Research or RMBR), National University of Singapore.

In addition to analyses done on all 176 sampled taxa (“Complete”), subsets of taxa were analyzed alone. A first subset (“Salticoida”) of 78 taxa highlighted the Salticoida, with just 7 non-salticoid outgroup taxa (4 hisponines, 1 spartaeine, 1 cocalodine, 1 lapsiine), in order to obtain an alignment that was less perturbed by highly divergent non-salticoids. A second subset highlighted the non-salticoids (“Non-salticoid”, 120 taxa), to obtain an alignment primarily for non-salticoid salticids, and also to be able to explore their relationships in more detail.

Gene choice and sequencing

Eight genes were used for this analysis. Two are nuclear ribosomal genes, 28s and 18s (Maddison and Hedin 2003, Maddison et al. 2008). Four are nuclear protein coding genes: actin 5C (Vink et al. 2008, Bodner and Maddison 2012), wingless (Blackledge et al. 2009), myosin heavy chain (“myosin HC”, Blackledge and Hayashi, unpublished), and histone 3 (Su et al. 2007). Two mitochondrial regions were also used, CO1 and another region including 16s and NADH1 ("16sND1", Hedin and Maddison 2001, Maddison and Hedin 2003). Following Bodner and Maddison (2012), the intron region of actin 5C was deleted from the analyses as it is highly variable and difficult to align.

The sequencing protocols for wingless and myosin HC are described below. For other genes, sequences marked “S” in Table 1 and Suppl. material 1 were obtained by the protocols of Su et al. (2007), all others by the protocols of Bodner and Maddison (2012) and Zhang and Maddison (2013).

For most wingless sequences, the forward and reverse primers used were respectively Spwgf1 and Spwgr1 (Blackledge et al. 2009). PCR amplification included a 2 min 94 °C denaturation and 35 cycles of 30 s at 94 °C, a 30 s annealing step at 52–57 °C, 30 s at 72 °C and one 3 min extension step at 72 °C. For some specimens this did not succeed in amplifying wingless, and for those we used a nested protocol starting with outer primers wg550F and wgABRz (Wild and Maddison 2008). The resulting product was then amplified using two internal primers, forward Wnt8MBf1 5’-TGTGCTACTCARACKTGYTGG-3’ and reverse Wnt8MBr3 5’-ACAAWGTTCTGCA ACTCATRCG-3’. For both the external and internal reactions amplification was done with 2 min 94 °C denaturation and 37 cycles of 20 s at 94 °C, a 20 s annealing step at 52 °C (wg550F/wgABRz) or 56 °C (wnt8MBf1/wnt8MBr3), and 2 min at 72 °C, and no final extension. The nested protocol obtained sequences for Bavia aff. aericeps (voucher d389), Hasarius adansoni (d295), Philodromus sp. (GR011), Simaetha sp. (d027), and Yllenus arenarius (JXZ173). In other specimens, the nested protocol often resulted in amplification of a different member of the wingless family (e.g. WNT-8), but these were readily detected (and excluded) by BLASTing them to other genes in the NCBI database (http://www.ncbi.nlm.nih.gov).

The region of myosin HC sequenced corresponds mostly to an intron. Primers used are (forward) Myhc1f 5'-ACAACAATTCTTCAACCATCAC-3' and (reverse) Myhc5r 5'-CTTCCTCAAGGATGGACA-3' (Blackledge and Hayashi, unpublished). PCR amplification included a 2 min 95 °C denaturation and 35 cycles of 20–45 s at 95 °C, a 45 s annealing step at 52 °C, 1 min at 72 °C and one 10 min extension step at 72 °C. The boundary between the exon and intron was determined by aligning the salticid implicit amino acid translations against the known transcript for myosin HC in Cyrtophora citricola (Genbank accession AAM97635.1; Ruiz-Trillo et al. 2002).

Two small single-nucleotide errors in the sequences were corrected after the analyses but before submission to Genbank. These are near the ends of CO1 of MRB199 (Gelotia sp. [Guangxi]) and MRB231 (Eburneana sp. [Gabon]). Given that CO1 had little resolution, these are unlikely to have affected the results.

Sequence alignment

Automatic multiple sequence alignment was performed by MAFFT (Katoh et al. 2002, 2005), run via the align package of Mesquite (prerelease of version 3, Maddison and Maddison 2014), aided by Mesquite for manual corrections and for alignment by amino acid. Coding regions were easily aligned by hand according to amino acid translations. This was done starting with an initial automated nucleotide alignment, followed by hand correction in Mesquite using the Color Nucleotide By Amino Acid function to reveal amino acid translation. Non-coding regions (28s, 18s, noncoding region of 16sND1, myosin HC intron) were aligned by MAFFT using the L-INS-i option (--localpair --maxiterate 1000). Mesquite was used to color the matrix via the option ‘‘Highlight Apparently Slightly Misaligned Regions’’ so as to identify regions that needed correction. These were almost always near the ends of sequences.

Alignment was done separately on the Complete, Non-salticoid and Salticoida datasets. Following the MAFFT alignment, the Salticoida dataset required 5 small realignments by hand in 18s. The first 60 positions in the initial alignment of 16s were also realigned locally, and in addition 8 minor shifts by one or two positions were made by hand. The Non-salticoid dataset required three simple hand fixes in 28s. The first 24 positions of 16s in the initial alignment were realigned by MAFFT in isolation because of several obvious misalignments. The Complete dataset appeared poorly aligned in 28s from sites 375 to 489 in the initial alignment, which were therefore realigned by MAFFT in isolation. The first 60 positions in the initial alignment of 16s were also realigned locally, and in addition 8 minor shifts by one or two positions were made by hand. Five small shifts were performed by hand for 18s. Many analyses were done with different variants of the alignments as this study was progressing, and the phylogenetic trees remained substantially consistent.

Phylogenetic analysis

Phylogenetic analyses using maximum likelihood were run using RAxML version 7.2.8alpha (Stamatakis 2006a, 2006b). The protein coding genes and 16sND1 were each divided into partitions. Protein coding regions were divided into one partition for 1st and 2nd codon positions, and another partition for third codon positions. Introns and non-coding regions were treated as separate partitions. For the fused 8 gene analyses, there were 7 partitions total: (1) 1st + 2nd codon positions in nuclear genes, (2) 3rd codon position nuclear, (3) nuclear intron, (4) nuclear ribosomal, (5) 1st + 2nd codon positions mitochondrial, (6) 3rd codon position mitochondrial, (7) noncoding mitochondrial. Each partition was permitted to have its own model parameters.

Analyses were done for each gene region separately with the Complete taxon set. In addition, analyses fusing all 8 genes were done for the Non-salticoid and Salticoida taxon sets. For all of these, RAxML runs assuming the GTRCAT model were used with 100 search replicates, to seek maximum likelihood trees. In addition, likelihood bootstrap analysis was performed with 500-1500 bootstrap replicates (as indicated in the figures), each involving a single search replicate. Phylogenetic analyses using GARLI version 1.0.699 (Zwickl 2006) under the model GTR+gamma+I were also done but are not reported; they resulted in substantially similar trees.

Data resources

The data underpinning the analyses reported in this paper are deposited in the Dryad Data Repository at doi: 10.5061/dryad.v53h1.

Results

Sequences obtained and used in analyses are indicated in Table 1 and Suppl. material 1, along with those sequences taken from the literature.

Figure 14 summarizes the results of the phylogenetic analyses, which are given in more detail in Figures 1527. Colors assigned to clades in Figure 14 are shown in the remaining figures. Figures 1519 show the All Genes results for the Complete, Non-salticoid and Salticoida datasets. Figures 2027 show the results for individual genes analyzed separately.

Figure 14.

Summary of phylogenetic results. Number above branch shows percentage of maximum likelihood bootstrap replicates with clade. For clades outside the Salticoida, these percentages come from the Non-salticoid dataset with 1500 replicates; within the Salticoida, these come from the Salticoida dataset with 1000 replicates; the Salticoida percentage comes from the Complete dataset with 1000 replicates. Long bar on branch shows same percentage graphically: black 91–100%; dark gray 81–90%; gray 71–80%; light gray 51–70%. Oval spots show presence of clade in maximum likelihood tree for individual genes, with exceptions noted by * and adjacent notes. The notes about wingless on the Spartaeinae node and actin on the Salticoida node are ambiguous in placement; they could equally well have been placed one node deeper because of missing data. Pale gray outline indicates no conclusion because of inadequate taxon sampling. All indications of support are from analyses excluding Eupoa, agoriines, Spartaeus spinimanus and “Spartaeusuplandicus. Bars show colors used to highlight taxa in Figs 1527.

Figure 15.

Phylogeny from complete taxon sample, All Genes analysis. Numbers beside branches show percentage of 1000 RAxML likelihood bootstrap replicates with clade in analysis with Eupoa and agoriines excluded. In analyses with these taxa included (500 bootstrap replicates), bootstrap percentages are within 5 of those shown, except for branches with two values (e.g. “100/60”), in which case the first value is from an analysis with Eupoa and agoriines excluded, the second value with them included. Colors of branches are the same as those highlighting taxa in Fig. 14.

Figures 16–17.

Phylogeny from Non-salticoid dataset, All Genes analysis. Numbers beside branches show percentage of RAxML likelihood bootstrap replicates with clade. 16 Non-salticoid analysis with all taxa included (1500 bootstrap replicates used) 17 Non-salticoid analysis with Eupoa, Spartaeus spinimanus, and “Spartaeusuplandicus excluded (500 bootstrap replicates used). Colors of branches are the same as those highlighting taxa in Fig. 14.

Figures 18–19.

Phylogeny from Salticoida dataset, All Genes analysis. 18 Salticoida analysis with all taxa included 19 Salticoida analysis with Agorius and Synagelides excluded. Numbers beside branches show percentage of 1000 RAxML likelihood bootstrap replicates with clade. Colors of branches are the same as those highlighting taxa in Fig. 14.

Figures 20–22.

Phylogeny from gene regions analyzed alone, complete taxon sample. 20 28s 21 18s 22 wingless. Colors of branches are the same as those highlighting taxa in Fig. 14.

Figures 23–27.

Phylogeny from gene regions analyzed alone, complete taxon sample. 23 myosin HC 24 actin 5C 25 Histone 3 26 CO1 27 16sND1. Colors of branches are the same as those highlighting taxa in Fig. 14.

Several taxa stood out as being problematical, especially for nuclear ribosomal genes. Eupoa was not only difficult to sequence (Maddison et al. 2007) but its 28s and 18s genes stand as outliers in alignments, remarkably different from other salticids. The same holds for the agoriines Agorius and Synagelides and, in 28s, for the hasariine Diplocanthopoda. These sequences do not appear to be contaminants, as they BLAST in the NCBI database to salticids. In analyses with just 28s or 18s, these taxa tend to appear on long branches, wandering to different parts of the salticid phylogeny in different analyses, attaching themselves together and to clearly inappropriate relatives (e.g. within the pellenines, Fig. 21). This instability and unexpected placement are likely artifacts due to long branch attraction (Felsenstein 1978), possibly related to compositional bias (Hasegawa and Hashimoto 1993). Eupoa and the agoriines have the highest GC bias of the sample (0.72–0.78, compared to 0.60–0.69 for all other species) in 28s, and are similar outliers in 18s. With wingless, Eupoa appears on a normal-length branch (Fig. 22). However, the agoriines with wingless are on a long branch in an unlikely place, within the euophryines (Fig. 22). Their placement is unstable: in slight variants of the analyses they come out in other places. There is nothing obviously unusual about the wingless sequences in agoriines, but whatever has shifted the GC bias in the nuclear ribosomal genes might also be affecting the rest of the genome. When Eupoa and the agoriines are excluded from analyses, bootstrap percentages rise through much of the tree, suggesting their instability is adding noise to the other relationships in the tree. For this reason, the reported bootstrap percentages and other indications of support are generally those for analysis with Eupoa and the agoriines excluded. Diplocanthopoda was left in the bootstrap analyses, because CO1, actin 5C and 16sND1 all agree on a clear placement in the hasariines.

Discussion

Many of the salticid clades now recognized by molecular data had been previously recognized by morphological data. For instance, Wanless (1980, 1984, 1985) recognized the three distinct lyssomanine groups and the Spartaeinae. The Salticoida was strongly supported by many morphological characters (Maddison 1988, 1996, Maddison and Hedin 2003), except that the status of the hisponines was unclear. Wanless (1981) implicitly included the hisponines within the salticoids, while Maddison (1996) did not consider the hisponines in his listing of salticoid synapomorphies. Other groups whose previous formulation by morphology mostly or entirely matches their current boundaries by molecular data are the marpissines (Barnes 1958), euophryines (Prószyński 1976), amycines (Galiano 1968), heliophanines (Maddison 1987), dendryphantines (Maddison 1996), and plexippines (Maddison 1988). At the finer scale, morphological systematics gave us concepts for many genera that are concordant with more recent data.

However, the first molecular data for salticid phylogeny as a whole (Maddison and Hedin 2003) uncovered several unanticipated groups, including the Amycoida, Plexippoida, and Marpissoida. Further data revealed the Astioida and Aelurilloida (Maddison et al. 2008), and later the Saltafresia (Bodner and Maddison 2012). These are major groups within the Salticoida, each uniting several subfamilies.

Deepest relationships

Our results help resolve or add strength to relationships at the deepest level of salticid phylogeny. Wanless (1980) recognized three major subdivisions of lyssomanines: (1) the New World genera Lyssomanes and Chinoscopus, (2) the Asian Onomastus, and (3) the remaining Old World genera including Asemonea. He suggested these three groups are so distinct that they may not belong together. The molecular data agree: the three groups’ divisions are so deep that their relationships have not yet been recovered, and it is possible, even likely, that they do not form a monophyletic group. Different analyses give different results of the relationships of these three, with some showing the New World genera as sister to the spartaeine-lapsiine-cocalodine clade (as recovered by Su et al. 2007), other results showing Onomastus in that role, and others showing the three lyssomanine groups together.

Spartaeines, lapsiines and cocalodines form a clade (node 1, Fig. 14). Although Rodrigo and Jackson (1992) concluded that spartaeines, Holcolaetis and the Cocalodes group form a clade (they were unaware of lapsiines), our analysis provides the first support for such an arrangement – their analysis included only a single taxon outside the group, and therefore it could not speak to the monophyly of the group. Our new result is intuitively appealing, as it groups together all of the extant medium-sized generalized non-salticoids/non-hisponines that are typically brown or gray. However, these presumably are or could be plesiomorphic traits; there had been no obvious reason to expect the spartaeines, lapsiines and cocalodines should have fallen together. There is no known morphological synapomorphy of this clade.

Within this spartaeine-lapsiine-cocalodine clade, the subclade historically best known by morphology is Wanless’s (1984) narrow version of the Spartaeinae, delimited by the presence of a tegular furrow (Wanless 1984). The Spartaeinae sensu stricto is primarily Afro-Eurasian, with a few Australasian species. Outside of this clade, there are no clear morphological synapomorphies defining subclades, and yet there is a striking geographical pattern: all of the Neotropical species belong to a clade, thus forming the lapsiines, while all of the Australasian species belong to a clade, thus forming the cocalodines. It is unsatisfying that we lack morphological synapomorphies for the lapsiines or cocalodines. The data suggest that the lapsiines and cocalodines are sister groups, with spartaeines more distant (Fig. 14).

Our results continue to support the relationship of hisponines with the Salticoida (node 2, Fig. 14; Figs 1517; Maddison and Needham 2006, Bodner and Maddison 2012).

The placement of Eupoa remains unclear. As noted under Results, the 28s and 18s genes of Eupoa may be unreliable phylogenetically, although Maddison et al. 2007 found those genes to place Eupoa among non-salticoid salticids. In our results Eupoa likewise has no clear placement, except for being outside the clade of Salticoida + Hisponinae. This result appears in the Non-salticoid and Complete datasets, and with the separate analyses of wingless, CO1, and 16sND1.

Spartaeinae

Our results strongly support the monophyly of the Spartaeinae sensu Su et al. (2007), placing Holcolaetis and Sonoita together with the Spartaeinae in the narrow sense. This is concordant with Wanless’s (1985) hypothesis that Holcolaetis and Sonoita formed a clade with the spartaeines to the exclusion of Cocalodes. The analyses of Su et al. (2007) did not sample Sparbambus, Taraxella, Brettus or Meleon, but otherwise their results were largely concordant with ours, which are: (1) Phaeacius (with Sparbambus) diverge deep, (2) Yaginumanus is sister to Spartaeus, (3) Gelotia, Neobrettus, Brettus and Meleon are monophyletic, (4) Paracyrba and Cyrba are sisters, (5) Portia is sister to Cyrba and Paracyrba. There is strong support for Gelotia through Cyrba as a monophyletic group, and for their relationship with Cocalus. By our data the exact placements of Taraxella and Mintonia are unclear.

A few spartaeine taxa in our analyses were problematical in appearing unstable, having different placements by different analyses. One of these is Spartaeus spinimanus, for which we have only 16sND1 and CO1 data, both gene regions that appear to evolve too quickly for reliable phylogenetic placement at this level (Bodner and Maddison 2012, Zhang and Maddison 2013). The other is “Spartaeusuplandicus, whose 28s sequence appears strongly divergent from others. This sequence is from Maddison and Hedin (2003, as “unidentified spartaeine”, vouchers 185 and 186), and it groups “Spartaeusuplandicus with one species of Holcolaetis, against the placements by morphology, CO1 and 16sND1. There is a chance that this gene was mis-sequenced in “Spartaeusuplandicus. Because of the instability generated, we excluded Spartaeus spinimanus and “Spartaeusuplandicus from our analyses giving bootstrap results.

Because of the concordance of our phylogenetic results with those of Su et al. (2007), our phylogeny continues to support their conclusions on the stepwise evolution of a complex predatory strategy in spartaeines.

Deep Salticoid relationships

The Salticoida’s basal divergence places the primarily-Neotropical Amycoida as sister group to an unnamed clade (node 3, Fig. 14) that contains most of salticid diversity. This surprising result, first discovered by Maddison and Hedin (2003), had very strong support in the analyses of Bodner and Maddison (2012). We here add support from two new genes, wingless and myosin HC, both of which independently resolve both the Amycoida and its sister group as monophyletic.

There have been hints of a clade uniting the Marpissoida, Astioida and baviines (Bodner and Maddison 2012). In our analyses the clade does not receive bootstrap support above 50% in the Complete or Salticoida analyses. The maximum likelihood trees either show the three as monophyletic or not, depending on taxon inclusion and details of the analysis (e.g., Figs 15 and 18). At present we must conclude the relationship between these three and the Saltafresia is unresolved.

Astioida

The astioids as delimited by Maddison et al. (2008) continue to be resolved as a clade, with new support from myosin HC and wingless (Figs 18, 22, 23). Although the body form of Nungia resembles that of baviines and the marpissoid Metacyrba, our data clearly place it as an astioid.

Saltafresia

Bodner and Maddison (2012) proposed a clade, the Saltafresia, containing salticoids other than amycoids, astioids, baviines and marpissoids. They found this clade reasonably well supported – 0.78 likelihood bootstrap and 1.0 posterior probability – but no single gene supported it on its own. Our data here continue to support it when all genes are combined. Two genes support it separately, with the exception of single taxa: 28s (but Tisaniba is included) and wingless (but Phintella is excluded).

Hasarieae

Previous work had established Habrocestum and Chinattus as close relatives of Hasarius (Maddison et al. 2008). We here add several more genera to the group, all Asian. These are Gedea, Echeclus and Diplocanthopoda. The relationships among these genera are not clearly resolved except for a well-supported relationship between Hasarius and Echeclus (Figs 14, 19).

Salticinae

The relationship between Salticus and the Philaeus group proposed by Maddison et al. (2008) receives additional support from wingless, along with previously-demonstrated support from 28s and actin. With high posterior probabilities (Bodner and Maddison 2008) and reasonable likelihood bootstrap values (Figs 15, 19), and supported by different genes independently (Figs 20, 22, 24), this relationship can now be considered sufficiently secure that we here formally place the genera of the Philaeus group into a subfamily — the Salticinae. In addition to genera previously analyzed (Salticus, Philaeus, Carrhotus, Tusitala, Mogrus, and Pignus) the subfamily also includes Phaulostylus, which is related to Tusitala (Fig. 14).

Plexippoida + Aelurilloida + Leptorchesteae + Salticinae (Node 5)

A set of four major groups (plexippoids, aelurilloids, leptorchestines and the Salticinae) form a clade in our analyses (node 5, Fig. 14). This group is resolved in the All Genes analyses with high bootstrap values, and it appears, almost, in the independent analyses of each of three genes (18s, wingless, myosin HC). We say “almost” because three of the genes have one or two taxa missing from or added to the group (Fig. 14). While we believe the evidence is good that these form a clade, there is a possibility that the Euophryinae might also fall nested within it. For instance, in the analyses of Bodner and Maddison (2012) the euophryines were placed as sister to the plexippoids. In our analyses the Euophryinae is placed as sister to the Plexippoida + Aelurilloida + Leptorchesteae + Salticinae.

This major clade is almost entirely Afro-Eurasian, with the plexippoid Habronattus being the only exception with more than a handful of species (others are Pellenes, Sibianor, Evarcha, Phlegra, Paramarpissa and Salticus, each with fewer than 15 described New World species).

Euophryinae

The 14 euophryine taxa in the analyses are resolved strongly as a monophyletic group. This is a stronger test of monophyly than that of Zhang and Maddison (2013), because it includes additional genes and more non-euophryine taxa. The All Genes analyses, along with wingless and myosin HC individually, suggest that the euophryines are the sister group to node 5 (Fig. 14).

Agoriines

Morphologically, the antlike agoriines Agorius and Synagelides are puzzling, with strangely contorted legs and unusual genitalia (Szüts 2003, Logunov and Hereward 2006, Prószyński 2009). While they appear to be salticoids, morphology has given little guidance as to their placement. As noted already, their 28s and 18s genes appear anomalous, and give no clear indication as to their relationships. In the All Genes analysis their placement is ambiguous, though they appear to be salticoids. In an attempt to determine their placement, an additional analysis was done, using a dataset that included Agorius constrictus and a chimera of Synagelides cf. lushanensis and Synagelides cf. palpalis (to have a single Synagelides taxon with three genes). The aberrant nuclear ribosomal genes of agoriines were excluded from the analysis. The other taxa included were the 70 taxa having at least 4 genes other than CO1 and histone 3. A RAxML likelihood analyses placed Agorius and Synagelides within the sister group of the Amycoida (node 3, Figure 14) with high support (bootstrap percentage 88), but exactly where was highly unstable. Among the 100 likelihood non-bootstrap search replicates were 7 different placements: sister to leptorchestines, sister to baviines, sister to node 5 in Figure 14, sister to the Saltafresia, sister to astioids + marpissoids + baviines, sister to node 3, or sister to node 3 without the baviines. While a relationship with the leptorchestines is appealing, as it would allow their antlike body forms to be homologous, the best we can say at present is that agoriines likely belong within the sister group of amycoids (node 3).

Generic limits

Most of the genera for which we have multiple species – e.g., Asemonea, Portia, Mintonia, Phaeacius, Cyrba – are inferred to be monophyletic in our analyses, corroborating existing concepts based on morphology. The clearest exception is Tabuina, in which Tabuina rufa and the similar Tabuina aff. rufa fall apart from the type species Tabuina varirata, which had been anticipated as a possibility by Maddison (2009). Lyssomanes, Galianora, and Gelotia are reconstructed as paraphyletic, but in each case the bootstrap values are low.

The placement of cf. Phaeacius [Sarawak] as sister to Phaeacius, with strong molecular divergence from the other species, would justify establishing a new genus for it.

Behaviour of individual genes

Previous work (Maddison and Hedin 2003, Bodner and Maddison 2012) has suggested that 28s and actin 5C are phylogenetically informative to a reasonable degree for deeper salticid phylogeny, insofar as their results are concordant with summed genes analyses, morphological resemblances, and biogeographical patterns. 16sND1 is useful at the shallower levels (Hedin and Maddison 2001) but has difficulties recovering deeper relationships, while CO1 struggles through both shallow and deep levels (Maddison and Hedin 2003, Bodner and Maddison 2012).

One surprise in our analyses was the informative behaviour of CO1 in deeper relationships among the non-salticoid salticids. Although CO1 is almost nonsensical in its inferred relationships within the Salticoida, it succeeds in recovering the Spartaeinae, the Spartaeineae sensu Wanless, the lapsiines, and the Salticoida as monophyletic.

Two new genes added, wingless, myosin HC, both show clear concordance with the 28s and previous all genes analyses. Wingless supports many of the previously recognized clades, including the Salticoida, Amycoida, the sister clade to Amycoida, Plexippoida, Marpissoida (in part), Astioida (in part), Spartaeinae sensu Wanless, and lapsiines. We find it encouraging that a haphazardly chosen protein-coding gene, independent from 28s, supports previous molecular results in Salticidae. There are still, however, many aspects of salticid relationships yet to be resolved, such as the deepest relationships in the family, including the relationships among the three subgroups of lyssomanines, the placement of Eupoa and the agoriines, and the relationships among astioids, marpissoids, baviines and the Saltafresia. With the coming era of genomic data, we expect large quantities of new data will be available for exploring these relationships.

Acknowledgments

We thank David Maddison for obtaining the sequences of wingless and 28s in Lapsias bellavista and Lapsias guamani. Geneviéve Leduc-Robert and Teresa Maddison assisted with molecular laboratory work. We thank Todd Blackledge and Cheryl Hayashi for their unpublished protocols for myosin HC. Gustavo Ruiz, Martín Ramírez, and G.B. Edwards gave helpful comments on the manuscript. For assistance on the 2008 expedition to Papua New Guinea, we thank Stephen Richards, Bruce Beehler, William Thomas, Luc Fimo Tuki, Aislan Tama Wanakipa Indiaf, Pingisa Saiké, Yainé Ribson, Agustus Kore, Muse Opiango, Banak Gamui, Robert Sine, Conservation International, Porgera Joint Venture, and the PNG Department of Environment and Conservation (for more details, see Maddison 2009). For assistance on the 2010 expedition to Ecuador, we thank David Maddison, Mauricio Vega, Edyta Piascik. Marco Reyes, the Ecuadorian Ministry of the Environment and the Museum of Zoology of the Pontificia Universidad Católica de Ecuador. Dmitri Logunov assisted with identifications of the Lyssomanes, Gustavo Ruiz with the Hypaeus. We also thank the staff of the Centre for Behavioural Ecology and Evolution (CBEE, Hubei University) and of the Behavioural Ecology and Sociobiology Lab (DBS, NUS) for all their help and support throughout this study, in particularly Jian Chen, Zhanqi Chen, Xiaoguo Jiao, Jie Liu, Yu Peng, Xiaoyan Wang, and Zengtao Zhang. This work was supported by an NSERC Discovery grant to WPM, and a NSFC grant (31272324) as well as a Singapore Ministry of Education (MOE) AcRF grant (R-154-000-591-112) to DL.

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Supplementary material 1

Specimens used in phylogenetic analyses, with localities and GenBank numbers of sequences indicated.

Authors: Wayne Maddison, Daiqin Li, Melissa Bodner, Junxia Zhang, Xu Xin, Qinqing Liu, Fengxiang Liu

Data type: Occurence; geographic locality; sex.

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.