Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Patterns of habitat affinity and Austral/Holarctic parallelism in dictynoid spiders (Araneae : Entelegynae)

Joseph C. Spagna A D , Sarah C. Crews B C and Rosemary G. Gillespie B
+ Author Affiliations
- Author Affiliations

A Department of Biology, William Paterson University, 300 Pompton Road, Wayne, NJ 07470, USA.

B Division of Organisms and Environment, University of California, Berkeley, 137 Mulford Hall, Berkeley, CA 94720-3114, USA.

C Present address: Berkeley City College, Department of Sciences, 2050 Center Street, Berkeley, CA 94709, USA.

D Corresponding author. Email: SpagnaJ@wpunj.edu

Invertebrate Systematics 24(3) 238-257 https://doi.org/10.1071/IS10001
Submitted: 8 January 2010  Accepted: 3 June 2010   Published: 30 August 2010

Abstract

The ability to survive in a terrestrial environment was a major evolutionary hurdle for animals that, once passed, allowed the diversification of most arthropod and vertebrate lineages. Return to a truly aquatic lifestyle has occurred only rarely among terrestrial lineages, and is generally associated with modifications of the respiratory system to conserve oxygen and allow extended periods of apnea. Among chelicerates, in particular spiders, where the circulatory system also serves as a hydrostatic skeleton, very few taxa have exploited aquatic environments, though these environments are abundant and range from freshwater ponds to the marine intertidal and relictual (salt) lakes. The traditional systematic positions of the taxa inhabiting these environments are controversial. Partitioned Bayesian analysis using a doublet model for stems in the nearly complete 18S rRNA gene (~1800 nt) and in the D2 and D3 regions of the 28S rRNA gene (~690 nt), and standard models for loops and full protein-coding histone H3 (349 nt) partitions (totalling 3133 bp when aligned) of dictynoid spiders and related lineages revealed that the only truly aquatic spider species, Argyroneta aquatica (Clerck, 1767) (Cybaeidae Banks, 1892), belongs in a clade containing other taxa with unusual habitat affinities related to an aquatic existence, including occupation of semi-aquatic (intertidal) areas (Desidae Pocock, 1985: Paratheuma spp.) and highly alkaline salt-crusts (Dictynidae O. Pickard-Cambridge, 1871: Saltonia incerta (Banks, 1898)). In a contrasting pattern, other spiders that also occupy intertidal zones, including some other members of the family Desidae (Desis spp., Badumna longinqua (L. Koch, 1867)), are an independently derived clade found primarily in the southern hemisphere. Use of the doublet model reduced some branch-support values in the single-gene trees for rRNA data, but resulted in a robust combined-data phylogeny from 18S rRNA, 28S rRNA, and histone H3. This combination of results – reduction in support in single-gene trees and gain in support in combined-data trees –is consistent with use of the doublet model reducing problematic signal from non-independent base pairs in individual data partitions, resulting in improved resolution in the combined-data analyses.

Additional keywords: Argyroneta, Cybaeidae, Desidae, Dictynoidea, doublet modelling, intertidal habitats, Paratheuma, partitioned Bayesian analysis, Saltonia, secondary structure.


Acknowledgements

The authors would like to thank Charles Griswold, Joel Ledford and Brent Opell for loan of specimens crucial to this work. All new specimens were collected under appropriate permits. We thank Jim McGuire and Matt Brandley for use of and assistance with computing resources at UCB, and Mark Miller and Lucie Chan for assistance with the CIPRES web portal. We thank David Gilley for comments leading to many improvements in the manuscript. Funding for the project was provided by the Schlinger Foundation, with additional support from the Division of Insect Biology at UC Berkeley and the National Science Foundation (Grant # DGE 0231877).


References


Angelini D. R., Jockusch E. L. (2008) Relationships among pest flour beetles of the genus Tribolium (Tenebrionidae) inferred from multiple molecular markers. Molecular Phylogenetics and Evolution 46, 127–141.
CrossRef | PubMed |

Ayoub N. A., Riechert S. E. (2004) Molecular evidence for Pleistocene glacial cycles driving diversification of a North American desert spider, Agelenopsis aperta. Molecular Ecology 13, 3453–3465.
CrossRef | PubMed |

Ayoub N. A., Garb J. E., Hedin M., Hayashi C. Y. (2007) Utility of the nuclear protein-coding gene, elongation factor-1 gamma (EF-1γ), for spider systematics, emphasizing family level relationships of tarantulas and their kin (Araneae: Mygalomorphae). Molecular Phylogenetics and Evolution 42, 394–409.
CrossRef | PubMed |

Beatty J. A., Berry J. W. (1988a) The spider genus Paratheuma Bryant (Araneae, Desidae). The Journal of Arachnology 16, 47–54.

Beatty J. A., Berry J. W. (1988b) Four new species of Paratheuma (Araneae, Desidae) from the Pacific. The Journal of Arachnology 16, 339–347.

Bennett R. G. (1991). ‘The Systematics of the North American Cybaeid Spiders (Araneae, Dictynoidea, Cybaeidae).’ (University of Guelph: Guelph, Ontario.)

Bergsten J. (2005) A review of long-branch attraction. Cladistics 21, 163–193.
CrossRef |

Bernhart S., Hofacker I., Will S., Gruber A., Stadler P. (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinformatics 9, 474.
CrossRef | PubMed |

Blackledge T. A., Scharff N., Coddington J. A., Szüts T., Wenzel J. W. , et al . (2009) Reconstructing web evolution and spider diversification in the molecular era. Proceedings of the National Academy of Sciences of the United States of America 106, 5229–5234.
CrossRef | PubMed |

Brandley M. C., Shmitz A., Reeder T. W. (2005) Partitioned Bayesian analyses, partition choice, and the phylogeny of scincid lizards. Systematic Biology 54, 373–390.
CrossRef | PubMed |

Chamberlin R. V., Gertsch W. J. (1958) The spider family Dictynidae in America north of Mexico. Bulletin of the American Museum of Natural History 116, 1–152.

Coddington J. A., Levi H. W. (1991) Systematics and evolution of spiders (Araneae). Annual Review of Ecology and Systematics 22, 565–592.
CrossRef |

Coddington J. A. , Giribet G. , Harvey M. S. , Prendini L. , and Walter D. E. (2004). Arachnida. In ‘Assembling the Tree of Life’. (Eds J. Cracraft and M. Donoghue.) pp. 296–318. (Oxford University Press: New York.)

Colgan D., McLauchlan A., Wilson G., Livingston S. (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
CrossRef |

Crews S. C., Puente-Rolon A. R., Rutstein E., Gillespie R. G. (2010) A comparison of populations of island and adjacent mainland species of Caribbean Selenops (Araneae: Selenopidae) spiders. Molecular Phylogenetics and Evolution 54, 970–983.
CrossRef | PubMed |

Deans A. R., Gillespie J. J., Yoder M. J. (2006) An evaluation of ensign wasp classification (Hymenoptera: Evaniidae) based on molecular data and insights from ribosomal RNA secondary structure. Systematic Entomology 31, 517–528.
CrossRef |

Dixon M. T., Hillis D. M. (1993) Ribosomal-RNA secondary structure – compensatory mutations and implications for phylogenetic analysis. Molecular Biology and Evolution 10, 256–267.
PubMed |


Eberhard W. G. (1990) Function and phylogeny of spider webs. Annual Review of Ecology and Systematics 21, 341–372.
CrossRef |

Edgar R. C. (2004) MUSCLE: multiple sequence alignment with accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
CrossRef | PubMed |

Erpenbeck D., Nichols S. A., Voigt O., Dohrmann M., Degnan B. M. , et al . (2007) Phylogenetic analyses under secondary structure-specific substitution models outperform traditional approaches: case studies with diploblast LSU. Journal of Molecular Evolution 64, 543–557.
CrossRef | PubMed |

Fares M. A., Byrne K. P., Wolfe K. H. (2006) Rate asymmetry after genome duplication causes substantial long-branch attraction artifacts in the phylogeny of saccharomyces species. Molecular Biology and Evolution 23, 245–253.
CrossRef | PubMed |

Felsenstein J. (1978) Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27, 401–410.
CrossRef |

Foelix R. F. (1996). ‘Biology of Spiders.’ 2nd edn. (Oxford University Press: New York.)

Forster R. R. (1987) A review of the spider superfamilies Hypochiloidea and Austrochiloidea (Araneae, Araneomorphae). Bulletin of the American Museum of Natural History 185, 1–116.

Forster R. R. , and Forster L. (1999). ‘Spiders of New Zealand and Their Worldwide Kin.’ (University of Otago Press: Dunedin.)

Forster R. R., Gray M. R. (1979) Progradungula, a new cribellate genus of the spider family Gradungulidae (Araneae). Australian Journal of Zoology 27, 1051–1071.
CrossRef |

Forster R. R., Wilton C. L. (1973) The spiders of New Zealand. Part IV. Otago Museum Bulletin 4, 1–309.

Gillespie J. J., Cannone J., Gutell R., Cognato A. I. (2004) A secondary structural model of the 28S rRNA expansion segments D2 and D3 from rootworms and related leaf beetles (Coleoptera: Chrysomelidae; Galerucinae). Insect Molecular Biology 13, 495–518.
CrossRef | PubMed |

Giribet G., Carranza S., Baguña N., Riutort M., Ribera C. (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
PubMed |


Givnish T. J. , and Systma K. J. (Eds) (1997). ‘Molecular Evolution and Adaptive Radiation.’ (Cambridge University Press: Cambridge, UK.)

Glesne R. (1998). Terrestrial riparian arthropod investigations in the Big Beaver Creek Research Natural Area, North Cascades National Park Service Complex, 1995–1996: Part III, Arachnida: Araneae. Technical Report NPS/NRNOCA/NRTR/98-03. United States Department of Interior – National Park Service – Pacific West Region.

Gowri-Shankar V. , and Jow H. (2006). PHASE: A Software Package for Phylogenetics and Sequence Evolution; Manual version 2.0: Available at: http://www.cs.manchester.ac.uk/ai/Software/phase/phase-2.0-manual.pdf [Accessed 1 October 2009].

Griswold C. E., Coddington J. A., Platnick N. I., Forster R. R. (1999) Towards a phylogeny of entelegyne spiders (Araneae, Araneomorphae, Entelegynae). The Journal of Arachnology 27, 53–63.

Griswold C. E., Ramirez M. J., Coddington J. A., Platnick N. I. (2005) Atlas of phylogenetic data for entelegyne spiders. Proceedings of the California Academy of Sciences 56(Suppl. II), 1–324.

Hagley E. A. C., Allen W. R. (1989) Prey of the cribellate spider Dictyna annulipes (Araneae: Dictynidae), on apple tree foliage. The Journal of Arachnology 17, 366–377.

Hedin M. C., Maddison W. P. (2001) A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae). Molecular Phylogenetics and Evolution 18, 386–403.
CrossRef | PubMed |

Hendriks L., Van Broeckhoven C., Vandenberghe A., Van de Peer Y., De Wachter R. (1988) Primary and secondary structure of the 18S ribosomal RNA of the bird spider Eurypelma californica and evolutionary relationships among eukaryotic phyla. European Journal of Biochemistry 177, 15–20.
CrossRef | PubMed |

Hofacker I. L., Fekete M., Stadler P. F. (2002) Secondary structure prediction for aligned RNA sequences. Journal of Molecular Biology 319, 1059–1066.
CrossRef | PubMed |

Huelsenbeck J. P., Rannala B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53, 904–913.
CrossRef | PubMed |

Huelsenbeck J. P., Ronquist F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
CrossRef | PubMed |

Humphreys W. F. (2006) Aquifers: the ultimate groundwater-dependent ecosystems. Australian Journal of Botany 54, 115–132.
CrossRef |

Jeram A. J., Selden P. A., Edwards D. (1990) Land Animals in the Silurian: arachnids and myriapods from Shropshire, England. Science 250, 658–661.
CrossRef | PubMed |

Kelchner S. A., Thomas M. A. (2007) Model use in phylogenetics: nine key questions. Trends in Ecology & Evolution 22, 87–94.
CrossRef |

Kim S., Kjer K. M., Duckett C. N. (2003) Comparison between molecular and morphological-based phylogenies of galerucine/alticine leaf beetles. Insect Systematics & Evolution 34, 53–64.

Kjer K. M. (1995) Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. Molecular Phylogenetics and Evolution 4, 314–330.
CrossRef | PubMed |

Kjer K. M. (2004) Aligned 18S and insect phylogeny. Systematic Biology 53, 506–514.
CrossRef | PubMed |

Kolaczkowski B., Thornton J. W. (2009) Long-branch attraction bias and inconsistency in Bayesian phylogenetics. PLoS ONE 4, e7891.
CrossRef | PubMed |

Lee M. S. Y. (1998) Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships. Biological Journal of the Linnean Society. Linnean Society of London 65, 369–453.
CrossRef |

Lehtinen P. (1967) Classification of the cribellate spiders and some allied families. Annales Zoologici Fennici 5, 199–468.

MacNaughton R., Cole J., Dalrymple R., Braddy S., Briggs D., Lukie T. (2002) First steps on land: arthropod trackways in Cambrian-Ordovician eolian sandstone, southeastern Ontario, Canada. Geology 30, 391–394.
CrossRef |

Maddison W. P., Hedin M. C. (2003) Jumping spider phylogeny. Invertebrate Systematics 17, 529–549.
CrossRef |

Mallatt J. M., Garey J. R., Shultz J. W. (2004) Ecdysozoan phylogeny and Bayesian inference first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Molecular Phylogenetics and Evolution 31, 178–191.
CrossRef | PubMed |

Martins E. P. (2000) Adaptation and the comparative method. Trends in Ecology & Evolution 15, 296–299.
CrossRef |

Mathews D. H. (2010). RNA Structure, version 5.03. Available at http://rna.urmc.rochester.edu/RNAstructure.html

Mathews D. H., Turner D. H. (2002) Dynalign: an algorithm for finding the secondary structure common to two RNA sequences. Journal of Molecular Biology [Verified July 2010]. 317, 191–203.
CrossRef | PubMed |

McQueen D. J., McLay C. L. (1983) How does the intertidal spider Desis marina (Hector) remain under water for such a long time? New Zealand Journal of Zoology 10, 383–392.

Miller M. A. , Holder M. T. , Vos R. , Midford P. E. , Liebowitz T. , Chan L. , Hoover P. , and Warnow T. (2009). ‘The CIPRES Portals.’ Available at http://www.phylo.org/sub_sections/portal [Accessed 23 December 2009].

Miller J. A., Carmichael A., Ramírez M. J., Spagna J. C., Haddad C. R., Rezac M., Johannesen J., Kral J., Wang X.-P., Griswold C. E. (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). Molecular Phylogenetics and Evolution 55, 786–804.
CrossRef | PubMed |

Murphy N. P., Framenau V. W., Donnellan S. C., Harvey M. S., Park Y.-C., Austin A. D. (2006) Phylogenetic reconstruction of the wolf spiders (Araneae: Lycosidae) using sequences from the 12S rRNA, 28S rRNA, and NADH1 genes: implications for classification, biogeography, and the evolution of web building behavior. Molecular Phylogenetics and Evolution 38, 583–602.
CrossRef | PubMed |

Nylander J. A. A. (2004). ‘MrModeltest (Version 2.2).’ Program distributed by the author. Uppsala University. Available at http://www.abc.se/~nylander/mrmodeltest2/mrmodeltest2.html [Verified July 2010].

Opell B. D. (1999) Changes in spinning anatomy and thread stickiness associated with the origin of orb-weaving spiders. Biological Journal of the Linnean Society. Linnean Society of London 68, 593–612.
CrossRef |

Penney D. (2003) Does the fossil record of spiders track that of their principal prey, the insects? Transactions of the Royal Society of Edinburgh. Earth Sciences 94, 275–281.
CrossRef |

Penney D., Ortuño V. M. (2006) Oldest true orb-weaving spider (Araneae: Araneidae). Biology Letters 2, 447–450.
CrossRef | PubMed |

Penney D., Wheater C. P., Selden P. A. (2003) Resistance of spiders to Cretaceous–Tertiary extinction events. Evolution 57, 2599–2607.
PubMed |


Pisani D., Poling L. L., Lyons-Weilier M., Hedges S. B. (2004) The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biology 2, 1–10.
CrossRef | PubMed |

Platnick N. I. (2010). The world spider catalog version 10.5. American Museum of Natural History, Available at http://research.amnh.org/entomology/spiders/catalog/index.html [Accessed April 10 2010].

Poinar G., Kerp H., Hass H. (2007) Palaeonema phyticum gen. n., sp. n. (Nematoda: Palaeonematidae fam. n.), a Devonian nematode associated with early land plants. Nematology 10, 9–14.

Posada D., Buckley T. R. (2004) Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.
CrossRef | PubMed |

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). Molecular Phylogenetics and Evolution 46, 1031–1048.
CrossRef | PubMed |

Ronquist F., Huelsenbeck J. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
CrossRef | PubMed |

Roth V. D. (1967) A review of the South American spiders of the family Agelenidae (Arachnida, Araneae). Bulletin of the American Museum of Natural History 134, 297–346.

Roth V. D., Brown W. L. (1975a) A new genus of Mexican intertidal zone spider (Desidae) with biological and behavioral notes. American Museum Novitates 2568, 1–7.

Roth V. D., Brown W. L. (1975b) Comments on the spider Saltonia incerta Banks (Agelenidae?). The Journal of Arachnology 3, 53–56.

SantaLucia J. J. (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proceedings of the National Academy of Sciences of the United States of America 95, 1460–1465.
CrossRef | PubMed |

Schöniger M., von Haeseler A. (1994) A stochastic model for the evolution of autocorrelated DNA sequences. Molecular Phylogenetics and Evolution 3, 240–247.
CrossRef | PubMed |

Selden P. A. (1990). Terrestrialization: invertebrates. In ‘Paleobiology: A Synthesis’. (Eds D. E. G. Briggs and P. R. Crowther.) pp. 64–68. (Blackwell: Oxford, UK.)

Selden P. A. (2002) Missing links between Argyroneta and Cybaeidae revealed by fossil spiders. The Journal of Arachnology 30, 189–200.
CrossRef |

Shirtcliffe N. J., McHale G., Newton M. I., Perry C. C., Pyatt F. B. (2006) Plastron properties of superhydrophobic surface. Applied Physics Letters 89, 104–106.
CrossRef |

Simon E. (1892). ‘Histoire naturelle des araignees (Vol. 1).’ (Paris.)

Spagna J. C., Gillespie R. G. (2006) Unusually long Hyptiotes (Araneae: Uloboridae) sequence for small subunit (18S) ribosomal RNA supports secondary structure model utility in spiders. The Journal of Arachnology 34, 557–565.
CrossRef |

Spagna J. C., Gillespie R. G. (2008) More data, fewer shifts: molecular insights into the evolution of the spinning apparatus in non-orb-weaving spiders. Molecular Phylogenetics and Evolution 46, 347–368.
CrossRef | PubMed |

Stamatakis A. (2006a) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
CrossRef | PubMed |

Stamatakis A. (2006 b). Phylogenetic models of rate heterogeneity: a high performance computing perspective. In ‘Proceedings of the 20th IEEE/ACM International Parallel and Distributed Processing Symposium (IPDPS2006), Rhodos, Greece’ .

Stamatakis A., Hoover P., Rougemont J. (2008) A fast bootstrapping algorithm for the RAxML web-servers. Systematic Biology 57, 758–771.
CrossRef | PubMed |

Thomas B. A. (1972) A probable moss from the Lower Carboniferous of the Forest of Dean, Gloucestershire. Annals of Botany 36, 155–161.

Thorp J. H. , and Kovich A. P. (1991). ‘Ecology and Classification of North American Freshwater Invertebrates.’ (Academic Press: New York.)

Tsagkogeorga G., Turon X., Hopcroft R. R., Tilak M. K., Feldstein T. , et al . (2009) An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evolutionary Biology 9, 187.
CrossRef | PubMed |

Ubick D. , Paquin P. , Cushing P. E. , and Roth V. (2005). ‘Spiders of North America: An Identification Manual.’ (American Arachnological Society: Gainesville, FL.)

Wake D. B. (1991) Homoplasy: the result of natural selection, or evidence of design limitations? American Naturalist 138, 543–567.
CrossRef |

Wheeler W. C., Hayashi C. Y. (1998) The phylogeny of the extant chelicerate orders. Cladistics 14, 173–192.
CrossRef |

Wheeler W. C., Whiting M. F., Carpenter J. C., Wheeler Q. D. (2001) The phylogeny of the insect orders. Cladistics 12, 1–57.
CrossRef |

Wilgenbusch J. C. , Warren D. L. , and Swofford D. L. (2004). AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Available at http://king2.scs.fsu.edu/CEBProjects/awty/awty_start.php [Accessed 1 May 2008].

Wise D. H. (1993). ‘Spiders in Ecological Webs.’ (Cambridge University Press: Cambridge, UK.)

Zuker M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 3406–3415.
CrossRef | PubMed |










Appendix 1.  Specimen and genetic data information for exemplars used
N.S. indicates no sequence was available for a particular locus
Click to zoom



Appendix 2.  Primers used
Click to zoom



Rent Article (via Deepdyve) Export Citation Cited By (10)

View Altmetrics