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: Biological Sciences

Volumn 279, Issue 1732, 2012, Pages 1341-1350

  Dimitrov, Dimitar ^a,f   Lopardo, Lara ^b   Giribet, Gonzalo ^c   Arnedo, Miquel A ^d   Álvarez Padilla, Fernando ^e   Hormiga, Gustavo ^f  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Zoologisches Institut und Museum   (Germany)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

^e UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^f GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Molecular dating; Spider diversification; Taxon sampling; Web evolution

Indexed keywords

BIOTIC FACTOR; EVOLUTIONARY BIOLOGY; GENETIC MARKER; JURASSIC; MOLECULAR ANALYSIS; PALEONTOLOGY; PHYLOGENETICS; PHYLOGENY; SAMPLING; SPIDER; TAXONOMY; TRIASSIC;

ARANEAE; ARANEIDAE;

EID: 84857531956     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.2011     Document Type: Article

References (85)

1. Selden, P. A., Shear, W. A. & Sutton, M. D. 2008 Fossil evidence for the origin of spider spinnerets, and a proposed arachnid order. Proc. Natl Acad. Sci. USA 105, 20 781-20 785. (doi:10.1073/pnas.0809174106)
2. Brunetta, L. & Craig, C. L. 2010 Spider silk: evolution and 400 million years of spinning, waiting, snagging, and mating. New Haven, CT: Yale University Press.
3. Vollrath, F. & Selden, P. 2007 The role of behavior in the evolution of spiders, silks, and webs. Annu. Rev. Ecol. Evol. Syst. 38, 819-846. (doi:10.1146/annurev.ecolsys.37.091305.110221)
4. Chacon, P. & Eberhard, W. G. 1980 Factors affecting numbers and kinds of prey caught in artificial spider webs, with considerations of how orb webs trap prey. Bull. Br. Arachnol. Soc. 5, 29-38.
5. Peñalver, E., Grimaldi, D. A. & Delclòs, X. 2006 Early Cretaceous spider web with its prey. Science 312, 1761-1761. (doi:10.1126/science.1126628)
6. Selden, P. A. 1989 Orb-web weaving spiders in the Early Cretaceous. Nature 340, 711-713. (doi:10.1038/340711a0)
7. Selden, P. A. & Penney, D. 2010 Fossil spiders. Biol. Rev. 85, 171-206. (doi:10.1111/j.1469-185X.2009.00099.x)
8. Selden, P. A., Shih, C. & Ren, D. 2011 A golden orbweaver spider (Araneae: Nephilidae: Nephila) from the Middle Jurassic of China. Biol. Lett. 7, 775-778. (doi:10.1098/rsbl.2011.0228)
9. Eberhard, W. G. 1982 Behavior of arachnids. Science 216, 876-877. (doi:10.1126/science.216.4548.876)
10. Hawthorn, A. C. & Opell, B. D. 2002 Evolution of adhesive mechanisms in cribellar spider prey capture thread: evidence for van der Waals and hygroscopic forces. Biol. J. Linn. Soc. 77, 1-8. (doi:10.1046/j.1095-8312.2002.00099.x)
11. Hawthorn, A. C. & Opell, B. D. 2003 van der Waals and hygroscopic forces of adhesion generated by spider capture threads. J. Exp. Biol. 206, 3905-3911. (doi:10.1242/jeb.00618)
12. Opell, B. D. & Bond, J. E. 2000 Capture thread extensibility of orb-weaving spiders: testing punctuated and associative explanations of character evolution. Biol. J. Linn. Soc. 70, 107-120. (doi:10.1111/j.1095-8312.2000.tb00203.x)
13. Opell, B. D. 1998 Economics of spider orb-webs: the benefits of producing adhesive capture thread and of recycling silk. Funct. Ecol. 12, 613-624. (doi:10.1046/j.1365-2435.1998.00222.x)
14. Blackledge, T. A. & Hayashi, C. Y. 2006 Unraveling the mechanical properties of composite silk threads spun by cribellate orb-weaving spiders. J. Exp. Biol. 209, 3131-3140. (doi:10.1242/jeb.02327)
15. Opell, B. D., Markley, B. J., Hannum, C. D. & Hendricks, M. L. 2008 The contribution of axial fiber extensibility to the adhesion of viscous capture threads spun by orb-weaving spiders. J. Exp. Biol. 211, 2243-2251. (doi:10.1242/jeb.016147)
16. Platnick, N. I. 2011 The world spider catalog, version 12.0. American Museum of Natural History. See http://research.amnh.org/iz/spiders/catalog/INTRO1.html. (doi:10.5531/db.iz.0001)
17. Craig, C. L., Bernard, G. D. & Coddington, J. A. 1994 Evolutionary shifts in the spectral properties of spider silks. Evolution 48, 287-296. (doi:10.2307/2410093)
18. Bond, J. E. & Opell, B. D. 1998 Testing adaptive radiation and key innovation hypotheses in spiders. Evolution 52, 403-414. (doi:10.2307/2411077)
19. Opell, B. D. 1997 The material cost and stickiness of capture threads and the evolution of orb-weaving spiders. Biol. J. Linn. Soc. 62, 443-458. (doi:10.1111/j.1095-8312.1997.tb01635.x)
20. Griswold, C. E., Coddington, J. A., Hormiga, G. & Scharff, N. 1998 Phylogeny of the orb-web building spiders (Araneae, Orbiculariae: Deinopoidea, Araneoidea). Zool. J. Linn. Soc. 123, 1-99. (doi:10.1111/j.1096-3642.1998.tb01290.x)
21. Benjamin, S. P. & Zschokke, S. 2003 Webs of theridiid spiders: construction, structure and evolution. Biol. J. Linn. Soc. 78, 293-305. (doi:10.1046/j.1095-8312.2003.00110.x)
22. Benjamin, S. P. & Zschokke, S. 2004 Homology, behaviour and spider webs: web construction behavior of Linyphia hortensis and L. triangularis (Araneae: Linyphiidae) and its evolutionary significance. J. Evol. Biol. 17, 120-130. (doi:10.1046/j.1420-9101.2004.00667.x)
23. Eberhard, W. G. 1977 Aggressive chemical mimicry by a bolas spider. Science 198, 1173-1175. (doi:10.1126/science.198.4322.1173)
24. Eberhard, W. G., Agnarsson, I. & Levi, H. W. 2008 Web forms and the phylogeny and theridiid spiders (Araneae: Theridiidae): chaos from order. Syst. Biodivers. 6, 415-475. (doi:10.1017/S1477200008002855)
25. Coddington, J. A. 1986 The genera of the spider family Theridiosomatidae. Smith. Contrib. Zool. 422, 1-96. (doi:10.5479/si.00810282.422)
26. Coddington, J. A. 1990 Cladistics and spider classification: Araneomorph phylogeny and the monophyly of orbweavers (Araneae: Araneomorphae, Orbiculariae). Acta Zool. Fenn. 190, 75-87.
27. Griswold, C. E., Ramírez, M. J., Coddington, J. A. & Platnick, N. I. 2005 Atlas of phylogenetic data for entelegyne spiders (Araneae: Araneomorphae: Entelegynae) with comments on their phylogeny. Proc. Calif. Acad. Sci. 56(Suppl. 2), 324.
28. Garb, J. E., Dimauro, T., Vo, V. & Hayashi, C. Y. 2006 Silk genes support the single origin of orb webs. Science 312, 1762. (doi:10.1126/science.1127946)
29. Blackledge, T. A., Scharff, N., Coddington, J. A., Szuts, T., Wenzel, J. W., Hayashi, C. Y. & Agnarsson, I. 2009 Reconstructing web evolution and spider diversification in the molecular era. Proc. Natl Acad. Sci. USA 106, 5229-5234. (doi:10.1073/pnas.0901377106)
30. Hausdorf, B. 1999 Molecular phylogeny of araneomorph spiders. J. Evol. Biol. 12, 980-985. (doi:10.1046/j.1420-9101.1999.00104.x)
31. Vink, C. J., Hedin, M., Bodner, M. R., Maddison, W. P., Hayashi, C. Y. & Garb, J. E. 2008 Actin 5C, a promising nuclear gene for spider phylogenetics. Mol. Phylogenet. Evol. 48, 377-382. (doi:10.1016/j.ympev.2008.03.003)
32. Miller, J. A. et al. 2010 Phylogeny of entelegyne spiders: affinities of the family Penestomidae (NEW RANK), generic phylogeny of Eresidae, and asymmetric rates of change in spinning organ evolution (Araneae, Araneoidea, Entelegynae). Mol. Phylogenet. Evol. 55, 786-804. (doi:10.1016/j.ympev.2010.02.021)
33. Pollock, D. D., Zwickl, D. J., McGuire, J. A. & Hillis, D. M. 2002 Increased taxon sampling is advantageous for phylogenetic inference. Syst. Biol. 51, 664-671. (doi:10.1080/10635150290102357)
34. Hillis, D. M., Pollock, D. D., McGuire, J. A. & Zwickl, D. J. 2003 Is sparse taxon sampling a problem for phylogenetic inference? Syst. Biol. 52, 124-126. (doi:10.1080/10635150390132911)
35. Zwickl, D. J. & Hillis, D. M. 2002 Increased taxon sampling greatly reduces phylogenetic error. Syst. Biol. 51, 588-598. (doi:10.1080/10635150290102339)
36. DeBry, R. W. 2005 The systematic component of phylogenetic error as a function of taxonomic sampling under parsimony. Syst. Biol. 54, 432-440. (doi:10.1080/10635150590946745)
37. Lopardo, L. & Hormiga, G. 2008 Phylogenetic placement of the Tasmanian spider Acrobleps hygrophilus (Araneae, Anapidae) with comments on the evolution of the capture web in Araneoidea. Cladistics 24, 1-33. (doi:10.1111/j.1096-0031.2007.00173.x)
38. Lopardo, L., Giribet, G. & Hormiga, G. 2011 Morphology to the rescue: molecular data and the signal of morphological characters in combined phylogenetic analyses-a case study from mysmenid spiders (Araneae, Mysmenidae), with comments on the evolution of web architecture. Cladistics 27, 278-330. (doi:10.1111/j.1096-0031.2010.00332.x)
39. Dimitrov, D. & Hormiga, G. 2011 An extraordinary new genus of spiders from Western Australia with an expanded hypothesis on the phylogeny of Tetragnathidae (Araneae). Zool. J. Linn. Soc. 161, 735-768. (doi:10.1111/j.1096-3642.2010.00662.x)
40. Hormiga, G. 2008 On the spider genus Weintrauboa (Araneae, Pimoidae), with a description of a new species fromChina and comments on its phylogenetic relationships. Zootaxa 1814, 1-20.
41. Regier, J. C. et al. 2009 Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evol. Biol. 9, 280. (doi:10.1186/1471-2148-9-280)
42. Zahiri, R., Kitching, I. J., Lafontaine, J. D., Mutanen, M., Kaila, L., LHolloway, J. D. & Wahlberg, N. 2011 A new molecular phylogeny offers hope for a stable family level classification of the Noctuoidea (Lepidoptera). Zool. Scr. 40, 158-173.
43. Katoh, K., Kuma, K., Toh, H. & Miyata, T. 2005 MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518. (doi:10.1093/nar/gki198)
44. Stamatakis, A. P., Meier, H. & Ludwig, T. 2008. RAxML: A parallel program for phylogenetic tree inference. See http://sco.h-its.org/exelixis/software.html.
45. Goloboff, P. A., Farris, J. S. & Nixon, K. C. 2008 TNT, a free program for phylogenetic analysis. Cladistics 24, 774-786. (doi:10.1111/j.1096-0031.2008.00217.x)
46. Wheeler, W. C. 1996 Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12, 1-9. (doi:10.1111/j.1096-0031.1996.tb00189.x)
47. A., Sy Vinh, L.& Wheeler, W. C. 2010 POYversion 4: phylogenetic analysis using dynamic homologies. Cladistics 26, 72-85. (doi:10.1111/j.1096-0031.2009.00282.x)
48. Thorley, J. L. & Wilkinson, M. 1999 Testing the phylogenetic stability of early tetrapods. J. Theor. Biol. 200, 343-344. (doi:10.1006/jtbi.1999.0999)
49. Wilkinson, M. 2006 Identifying stable reference taxa for phylogenetic nomenclature. Zool. Scr. 35, 109-112. (doi:10.1111/j.1463-6409.2005.00213.x)
50. Smith, S. A. & Dunn, C. W. 2008 Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24, 715-716. (doi:10.1093/bioinformatics/btm619)
51. Maddison, W. P. & Maddison, D. R. 2010 Mesquite: a modular system for evolutionary analysis. Version 2.73. See http://mesquiteproject.org.
52. Lewis, P. O. 2001 A likelihood approach to estimating phylogeny from discrete morphological characters data. Syst. Biol. 50, 913-925. (doi:10.1080/106351501753462876)
53. Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. 2006 Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88. (doi:10.1371/journal.pbio.0040088)
54. Drummond, A. J. & Rambaut, A. 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214. (doi:10.1186/1471-2148-7-214)
55. Agnarsson, I. 2004 Morphological phylogeny of cobweb spiders and their relatives (Araneae, Araneoidea, Theridiidae). Zool. J. Linn. Soc. 141, 447-626. (doi:10.1111/j.1096-3642.2004.00120.x)
56. Arnedo, M. A., Coddington, J., Agnarsson, I. & Gillespie, R. G. 2004 From a comb to a tree: phylogenetic relationships of the comb-footed spiders (Araneae, Theridiidae) inferred from nuclear and mitochondrial genes. Mol. Phylogenet. Evol. 31, 225-245. (doi:10.1016/S1055-7903(03)00261-6)
57. Kuntner, M., Coddington, J. A. & Hormiga, G. 2008 Phylogeny of extant nephilid orb-weaving spiders (Araneae, Nephilidae): testing morphological and ethological homologies. Cladistics 24, 147-217. (doi:10.1111/j.1096-0031.2007.00176.x)
58. K. 2003 Phylogeny of Symphytognathidae s.l. (Araneae, Araneoidea). Zool. Scri. 32, 129-151. (doi:10.1046/j.1463-6409.2003.00103.x)
59. Rix, M.G., Harvey, M. S.& Roberts, J.D. 2008 Molecular phylogenetics of the spider family Micropholcommatidae (Arachnida: Araneae) using nuclear rRNA genes (18S and 28S). Mol. Phylogenet. Evol. 46, 1031-1048. (doi:10.1016/j.ympev.2007.11.001)
60. Álvarez-Padilla, F., Dimitrov, D., Giribet, G. & Hormiga, G. 2009 Phylogenetic relationships of the spider family Tetragnathidae (Araneae, Araneoidea) based on morphological and DNA sequence data. Cladistics 25, 109-146.(doi:10.1111/j.1096-0031.2008.00242.x)
61. Ayoub, N. A., Garb, J. E., Hedin, M. & Hayashi, C. Y. 2007 Utility of the nuclear protein-coding gene, elongation factor-1 gamma (EF-1g), for spider systematics, emphasizing family level relationships of tarantulas and their kin (Araneae: Mygalomorphae). Mol. Phylogenet. Evol. 42, 394-409. (doi:10.1016/j.ympev.2006.07.018)
62. Steiper, M. E. & Young, N. M. 2008 Timing primate evolution: lessons from the discordance between molecular and paleontological estimates. Evol. Anthropol. 17, 179-188. (doi:10.1002/Evan.20177)
63. Penney, D. & Selden, P. A. 2002 The oldest linyphiid spider, in Lower Cretaceous Lebanese amber (Araneae, Linyphiidae, Linyphiinae). J. Arachnol. 30, 487-493. (doi:10.1636/0161-8202(2002)030[0487:TOLSIL]2.0.CO;2)
64. Eskov, K. 1984 A new fossil spider family from the Jurassic of Transbaikalia (Araneae: Chelicerata). Neues Jahrb. Geol. Palaeontol. Mon. hefte 1984, 645-653.
65. Eisner, T., Alsop, R. & Ettershank, G. 1964 Adhesiveness of spider silk. Science 146, 1058-1061. (doi:10.1126/science.146.3647.1058)
66. Penney, D. 2004 (for 2003 Does the fossil record of spiders track that of their principal prey, the insects? Trans. R. Soc. Edinb. Earth Sci. 94, 275-281.
67. Grimaldi, D. A. & Engel, M. S. 2005 Evolution of the insects. Cambridge, UK: Cambridge University Press.
68. Gastaldo, R. A., Stevanovic-Walls, I. M., Ware, W. N. & Greb, S. F. 2004 Community heterogeneity of early Pennsylvanian peat mires. Geology 32, 693-696. (doi:10.1130/G20515.1)
69. Looy, C. V., Twitchett, R. J., Dilcher, D. L., Konijnenburg-Van Cittert, J. H. A. & Visscher, H. 2001 Life in the end-Permian dead zone. Proc. Natl Acad. Sci. USA 98, 7879-7883. (doi:10.1073/pnas.131218098)
70. Hinz, J. K., Smith, I., Pfretzschner, H.-U., Wings, O. & Sun, G. 2010 A high-resolution three-dimensional reconstruction of a fossil forest (Upper Jurassic Shishugou Formation, Junggar Basin, Northwest China). Palaeobiodivers. Palaeoenviron. 90, 215-240. (doi:10.1007/s12549-010-0036-y)
71. Thorn, V. 2005 A Middle Jurassic fossil forest from New Zealand. Palaeontology 48, 1021-1039. (doi:10.1111/j.1475-4983.2005.00490.x)
72. Eberhard, W. G. 1990 Imprecision in the behavior of Leptomorphus sp. (Diptera, Mycetophilidae) and the evolutionary origin of new behavior patterns. J. Insect Behav. 3, 327-357. (doi:10.1007/BF01052113)
73. Eberhard, W. G. 2000 Breaking the mold: behavioral variation and evolutionary innovation in Wendilgarda spiders (Araneae Theridiosomatidae). Ethol. Ecol. Evol. 12, 223-235. (doi:10.1080/08927014.2000.9522797)
74. Lewis, P. O., Holder, M. T. & Holsinger, K. E. 2005 Polytomies and Bayesian phylogenetic inference. Syst. Biol. 54, 241-253. (doi:10.1080/10635150590924208)
75. Hillis, D. M. 1996 Inferring complex phylogenies. Nature 383, 130-131. (doi:10.1038/383130a0)
76. Wiens, J. J. 2006 Missing data and the design of phylogenetic analyses. J. Biomed. Inform. 39, 34-42. (doi:10.1016/j.jbi.2005.04.001)
77. Wiens, J. J. 2003 Missing data, incomplete taxa, and phylogenetic accuracy. Syst. Biol. 52, 528-538. (doi:10.1080/10635150390218330)
78. Wiens, J. J. 2005 Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Syst. Biol. 54, 731-742. (doi:10.1080/10635150500234583)
79. Wiens, J. J. & Moen, D. S. 2008 Missing data and the accuracy of Bayesian phylogenetics. J. Syst. Evol. 46, 307-314.
80. Goloboff, P. A., Catalano, S. A., Mirande, J. M., Szumik, C. A., Arias, J. S., Källersjö, M. & Farris, J. S. 2009 Phylogenetic analysis of 73 060 taxa corroborates major eukaryotic groups. Cladistics 25, 211-230. (doi:10.1111/j.1096-0031.2009.00255.x)
81. Dunn, C. W. et al. 2008 Broad taxon sampling improves resolution of the animal tree of life. Nature 452, 745-749. (doi:10.1038/nature06614)
82. Lee, M. S. Y. 2005 Choosing reference taxa in phylogenetic nomenclature. Zool. Scr. 34, 313-328. (doi:10.1111/j.1463-6409.2005.00196.x)
83. Giribet, G. & Edgecombe, G. D. 2006 Conflict between data sets and phylogeny of centipedes: an analysis based on seven genes and morphology. Proc. R. Soc. B 273, 531-538. (doi:10.1098/rspb.2005.3365)
84. Hejnol, A. et al. 2009 Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B 276, 4261-4270. (doi:10.1098/rspb.2009.0896)
85. Driskell, A. C., Ane, C., Burleigh, J. G., McMahon, M. M., O'Meara, B. C. & Sanderson, M. J. 2004 Prospects for building the tree of life from large sequence databases. Science 306, 1172-1174. (doi:10.1126/science.1102036)