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

Evolution of host use, group-living and foraging behaviours in kleptoparasitic spiders: molecular phylogeny of the Argyrodinae (Araneae : Theridiidae)

Yong-Chao Su A B C and Deborah Smith B
+ Author Affiliations
- Author Affiliations

A Department of Life Science, Tunghai University, No. 1727, Sec. 4, Taiwan Boulevard, Xitun District, Taichung 40704, Taiwan.

B Department of Ecology and Evolutionary Biology, Haworth Hall, 1200 Sunnyside Ave, University of Kansas, Lawrence, KS 66045, USA.

C Corresponding author. Email: ycsu527@gmail.com

Invertebrate Systematics 28(4) 415-431 https://doi.org/10.1071/IS14010
Submitted: 8 February 2014  Accepted: 23 April 2014   Published: 12 September 2014

Abstract

Spiders in the subfamily Argyrodinae are known for their associations with other spiders. These associations include predation (araneophagy), web usurpation and kleptoparasitism. Although the majority of the 239 described species are solitary, ~20 species live in groups in the webs of their hosts. We constructed a molecular phylogeny of argyrodine genera and species in order to investigate (1) the evolution of araneophagy and kleptoparasitism, and (2) group-living and its association with particular types of host webs. We investigated the phylogeny of 41 primarily Asian and American species representing six recognised genera of Argyrodinae, using sequences of four genes: mitochondrial cytochrome c oxidase I (COI) and 16S rRNA (16S); and nuclear 28S rRNA (28S) and histone 3 (H3). We used Bayesian methods to reconstruct the ancestral states of three behavioural characters: foraging method, group-living and specialisation on large webs of large hosts. We tested for correlated evolution of group-living behaviour and specialisation on large webs using reversible-jump Markov chain Monte Carlo methods. The molecular phylogenetic analyses support the monophyly of the Argyrodinae. Reconstruction of ancestral states shows the evolutionary pathway of web-invading behaviour in Argyrodinae is from araneophagy to kleptoparasitism, and then to group-living kleptoparasitism. We found the evolution of group-living behaviour is strongly correlated with specialisation on the use of large host webs, which provide a larger food resource than smaller webs.

Additional keywords: araneophagy, correlated character evolution, kleptoparasitism, sociality.


References

Agnarsson, I. (2002). Sharing a web – on the relation of sociality and kleptoparasitism in theridiid spiders (Theridiidae, Araneae). The Journal of Arachnology 30, 181–188.
Sharing a web – on the relation of sociality and kleptoparasitism in theridiid spiders (Theridiidae, Araneae).CrossRef |

Agnarsson, I. (2004). Morphological phylogeny of cobweb spiders and their relatives (Araneae, Araneoidea, Theridiidae). Zoological Journal of the Linnean Society 141, 447–626.
Morphological phylogeny of cobweb spiders and their relatives (Araneae, Araneoidea, Theridiidae).CrossRef |

Agnarsson, I., Avilés, L., Coddington, J. A., and Maddison, W. P. (2006). Sociality in Theridiid spiders: repeated origins of an evolutionary dead end. Evolution 60, 2342–2351.
Sociality in Theridiid spiders: repeated origins of an evolutionary dead end.CrossRef | 17236425PubMed |

Agnarsson, I., Maddison, W. P., and Avilés, L. (2007). The phylogeny of the social Anelosimus spiders (Araneae: Theridiidae) inferred from six molecular loci and morphology. Molecular Phylogenetics and Evolution 43, 833–851.
The phylogeny of the social Anelosimus spiders (Araneae: Theridiidae) inferred from six molecular loci and morphology.CrossRef | 1:CAS:528:DC%2BD2sXlvVOrurk%3D&md5=6e762f9f10b630e730a71b095b976637CAS | 17081775PubMed |

Arnedo, M. A., Coddington, J., Agnarsson, I., and 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. Molecular Phylogenetics and Evolution 31, 225–245.
From a comb to a tree: phylogenetic relationships of the comb-footed spiders (Araneae, Theridiidae) inferred from nuclear and mitochondrial genes.CrossRef | 1:CAS:528:DC%2BD2cXhvFSksL0%3D&md5=2ef99c8d40496eb79f3b464ccaabdffeCAS | 15019622PubMed |

Avilés, L. (1997). Causes and consequences of cooperation and permanent-sociality in spiders. In ‘The Evolution of Social Behavior in Insects and Arachnids’. (Ed. J. C. Choe and B. J. Crespi.) pp. 476–498. (Cambridge University Press: Cambridge.)

Baba, Y. G., Walters, R. J., and Miyashita, T. (2007). Host-dependent differences in prey acquisition between populations of a kleptoparasitic spider Argyrodes kumadai (Araneae: Theridiidae). Ecological Entomology 32, 38–44.
Host-dependent differences in prey acquisition between populations of a kleptoparasitic spider Argyrodes kumadai (Araneae: Theridiidae).CrossRef |

Bidegaray-Batista, L., and Arnedo, M. A. (2011). Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders. BMC Evolutionary Biology 11, 317.
Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders.CrossRef | 22039781PubMed |

Bilde, T., and Lubin, Y. (2011). Group living in spiders: cooperative breeding and coloniality. In ‘Spider Behavior: Flexibility and Versatility’. (Ed. M. E. Herberstein.) pp. 275–298. (Cambridge University Press: Cambridge.)

Brach, V. (1977). Anelosimus studiosus (Araneae: Theridiidae) and the evolution of quasisociality in theridiid spiders. Evolution 31, 154–161.
Anelosimus studiosus (Araneae: Theridiidae) and the evolution of quasisociality in theridiid spiders.CrossRef |

Buskirk, R. (1981). Sociality in the Arachnida. In ‘Social Insects. Vol. 2’. (Ed. H. R. Hermann.) pp. 281–367. (Academic Press: New York, NY.)

Cangialosi, K. R. (1997). Foraging versatility and the influence of host availability in Argyrodes trigonum (Araneae, Theridiidae). The Journal of Arachnology 25, 182–193.

Cobbold, S. M., and Su, Y. C. (2010). The host becomes dinner: possible use of Cyclosa as a nuptial gift by Argyrodes in a colonial web. The Journal of Arachnology 38, 132–134.
The host becomes dinner: possible use of Cyclosa as a nuptial gift by Argyrodes in a colonial web.CrossRef |

Colgan, D. J., McLauchlan, A., Edgecombe, G. D., Macaranas, J., Cassis, G., Gray, M. R., Livingston, S. P., and Wilson, G. D. F. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution.CrossRef |

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.CrossRef | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=beec25ccf0d2a98903aa512fd45babe5CAS | 22367748PubMed |

Eberhard, W. G. (1979). Argyrodes attenuatus (Theridiidae): a web that is not a snare. Psyche 86, 407–413.
Argyrodes attenuatus (Theridiidae): a web that is not a snare.CrossRef |

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.CrossRef | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=0f644003e0450eab42e285b06371fbb5CAS | 15034147PubMed |

Elgar, M. (1993). Inter-specific associations involving spiders: kleptoparasitism, mimicry and mutualism. Memoirs of the Queensland Museum 33, 411–430.

Evans, T. A. (1999). Kin recognition in a social spider. Proceedings of the Royal Society of London. Series B, Biological Sciences 266, 287–292.
Kin recognition in a social spider.CrossRef |

Evans, T. A., and Goodisman, M. A. D. (2002). Nestmate relatedness and population genetic structure of the Australian social crab spider Diaea ergandros (Araneae: Thomisidae). Molecular Ecology 11, 2307–2316.
Nestmate relatedness and population genetic structure of the Australian social crab spider Diaea ergandros (Araneae: Thomisidae).CrossRef | 1:CAS:528:DC%2BD38XptlSlsr0%3D&md5=cd54175746b8c327652727ce591333b5CAS | 12406241PubMed |

Exline, H., and Levi, H. (1962). American spiders of the genus Argyrodes (Araneae, Theridiidae). Bulletin of the Museum of Comparative Zoology. 127, 75–202.

Fernández Campón, F. (2007). Group foraging in the colonial spider Parawixia bistriata (Araneidae): effect of resource levels and prey size. Animal Behaviour 74, 1551–1562.
Group foraging in the colonial spider Parawixia bistriata (Araneidae): effect of resource levels and prey size.CrossRef |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=41891c10f444b637826cbf6001a4954cCAS | 7881515PubMed |

Fowler, H., and Gobbi, N. (1988). Cooperative prey capture by an orb-web spider. Naturwissenschaften 75, 208–209.
Cooperative prey capture by an orb-web spider.CrossRef |

Green, P. J. (1995). Reversible jump Markov chain Monte Carlo computation and Bayesian model determination. Biometrika 82, 711–732.
Reversible jump Markov chain Monte Carlo computation and Bayesian model determination.CrossRef |

Hedin, M. C. (1997). Speciational history in a diverse clade of habitat-specialized spiders (Araneae: Nesticidae: Nesticus): inferences from geographic-based sampling. Evolution 51, 1929–1945.
Speciational history in a diverse clade of habitat-specialized spiders (Araneae: Nesticidae: Nesticus): inferences from geographic-based sampling.CrossRef |

Hedin, M. C., and 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.
A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae).CrossRef | 1:CAS:528:DC%2BD3MXit1ansbg%3D&md5=cedf4973ea9822c87cf2bcd4c96f698aCAS | 11277632PubMed |

Hénaut, Y., Delme, J., Legal, L., and Williams, T. (2005). Host selection by a kleptobiotic spider. Naturwissenschaften 92, 95–99.
Host selection by a kleptobiotic spider.CrossRef | 15592806PubMed |

Kass, R. E., and Raftery, A. E. (1995). Bayes factors. Journal of the American Statistical Association 90, 773–795.
Bayes factors.CrossRef |

Koh, T. H., and Li, D. (2003). State dependent prey type preferences of a kleptoparasitic spider Argyrodes flavescens (Araneae: Theridiidae). Journal of Zoology 260, 227–233.
State dependent prey type preferences of a kleptoparasitic spider Argyrodes flavescens (Araneae: Theridiidae).CrossRef |

Kullmann, E. J. (1972). Evolution of social behavior in spiders (Araneae; Eresidae and Theridiidae). American Zoologist 12, 419–426.

Kuntner, M., Arnedo, M. A., Trontelj, P., Lokovšek, T., and Agnarsson, I. (2013). A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage. Molecular Phylogenetics and Evolution 69, 961–979.
A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage.CrossRef | 1:CAS:528:DC%2BC3sXhtFSmt77K&md5=f12200ce3dd52d6424ee263921a38694CAS | 23811436PubMed |

Lemey, P., Rambaut, A., Drummond, A. J., and Suchard, M. A. (2009). Bayesian phylogeography finds its roots. PLoS Computational Biology 5, e1000520.
Bayesian phylogeography finds its roots.CrossRef | 19779555PubMed |

Lubin, Y., and Bilde, T. (2007). The evolution of sociality in spiders. Advances in the Study of Behavior 37, 83–145.
The evolution of sociality in spiders.CrossRef |

Miyashita, T. (2002). Population dynamics of two species of kleptoparasitic spiders under different host availabilities. The Journal of Arachnology 30, 31–38.
Population dynamics of two species of kleptoparasitic spiders under different host availabilities.CrossRef |

Miyashita, T., Maezono, Y., and Shimazaki, A. (2004). Silk feeding as an alternative foraging tactic in a kleptoparasitic spider under seasonally changing environments. Journal of Zoology 262, 225–229.
Silk feeding as an alternative foraging tactic in a kleptoparasitic spider under seasonally changing environments.CrossRef |

Nylander, J. A. A., Wilgenbusch, J. C., Warren, D. L., and Swofford, D. L. (2008). AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24, 581–583.
AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics.CrossRef | 1:CAS:528:DC%2BD1cXitVKis7g%3D&md5=2cd588dbda07e498a2e2ce90171acfa8CAS |

Pagel, M., and Lutzoni, F. (2002). Accounting for phylogenetic uncertainty in comparative studies of evolution and adaptation. Biological Evolution and Statistical Physics Vol. 585. (Eds M. Lässig and A. Valleriani.) pp. 148–161. (Springer: Berlin.)

Pagel, M., and Meade, A. (2006). Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. American Naturalist 167, 808–825.
Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo.CrossRef | 16685633PubMed |

Penney, D., and Green, D. I. (2011). Fossils in Amber: Remarkable Snapshots of Prehistoric Forest Life. (Siri Scientific Press.) 226 pp.

Platnick, N. (2014). The world spider catalog, version 15 American Museum of Natural History. Available at http://research.amnh.org/iz/spiders/catalog/ [Verified July 2014]

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: phylogenetic model averaging.CrossRef | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=a227fa0ae4120a3a8c06cab96986f12aCAS | 18397919PubMed |

Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2013). Tracer v1.5. Available from http://beast.bio.ed.ac.uk/Tracer [Verified July 2014]

Robinson, M. H., and Robinson, B. (1973). Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea. Smithsonian Contributions to Zoology 149, 1–76.
Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea.CrossRef |

Roeloffs, R., and Riechert, S. E. (1988). Dispersal and population-genetic structure of the cooperative spider, Agelena consociata, in west African rainforest. Evolution 42, 173–183.
Dispersal and population-genetic structure of the cooperative spider, Agelena consociata, in west African rainforest.CrossRef |

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.CrossRef | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=d5b84f5cc16cfb75b367ced57a76cb2cCAS | 12912839PubMed |

Saaristo, M. I. (1978). Spiders (Arachnida, Araneae) from the Seychelle islands, with notes on taxonomy. Annales Zoologici Fennici 15, 99–126.

Saaristo, M. I. (2006). Theridiid or cobweb spiders of the granitic Seychelles islands (Araneae, Theridiidae). Phelsuma 14, 49–89.

Simon, E. (1864). ‘Histoire Naturelle des Araignées. First Edn.’ Librairie Encyclopédique de Roret, rue Hautefeuille, 12, Paris.

Simon, E. (1892–1895). ‘Histoire Naturelle des Araignées. Second Edn.’ Volume 1 (section 3, published 10 October 1894), Librairie Encyclopédique de Roret, rue Hautefeuille, 12, Paris, pp. 496–503.

Smith Trail, D. (1980). Predation by Argyrodes (Theridiidae) on solitary and communal spiders. Psyche 87, 349–355.
Predation by Argyrodes (Theridiidae) on solitary and communal spiders.CrossRef |

Smith, D. (1982). Reproductive success of solitary and communal Philoponella oweni (Araneae: Uloboridae). Behavioral Ecology and Sociobiology 11, 149–154.
Reproductive success of solitary and communal Philoponella oweni (Araneae: Uloboridae).CrossRef |

Smith, D. R., and Hagen, R. H. (1996). Population structure and interdemic selection in the cooperative spider Anelosimus eximius. Journal of Evolutionary Biology 9, 589–608.
Population structure and interdemic selection in the cooperative spider Anelosimus eximius.CrossRef |

Smith, D., Van Rijn, S., Henschel, J., Bilde, T., and Lubin, Y. (2009). Amplified fragment length polymorphism fingerprints support limited gene flow among social spider populations. Biological Journal of the Linnean Society. Linnean Society of London 97, 235–246.
Amplified fragment length polymorphism fingerprints support limited gene flow among social spider populations.CrossRef |

Tanaka, K. (1984). Rate of predation by a kleptoparasitic spider, Argyrodes fissifrons, upon a large host spider, Agelena limbata. The Journal of Arachnology 12, 363–367.

Tanikawa, A. (1998). The new synonymy of the spider genus Argyrodes (Araneae: Theridiidae) and a description of a new species from Japan. Acta Arachnologica 47, 21–26.
The new synonymy of the spider genus Argyrodes (Araneae: Theridiidae) and a description of a new species from Japan.CrossRef |

Uetz, G. W., and Hieber, C. S. (1997). Colonial web-building spiders: balancing the costs and benefits of group-living. In ‘Social Behavior in Insects and Arachnids’. (Eds J. C. Chou and B. J. Crespi.) pp. 458–475. (Cambridge University Press: Cambridge, UK.)

Vollrath, F. (1979). Behaviour of the kleptoparasitic spider Argyrodes elevatus (Araneae, Theridiidae). Animal Behaviour 27, 515–521.
Behaviour of the kleptoparasitic spider Argyrodes elevatus (Araneae, Theridiidae).CrossRef |

Whitehouse, M. (1988). Factors influencing specificity and choice of host in Argyrodes antipodiana (Theridiidae, Araneae). The Journal of Arachnology 16, 349–355.

Whitehouse, M. (1991). To mate or fight? Male-male competition and alternative mating strategies in Argyrodes antipodiana (Theridiidae, Araneae). Behavioural Processes 23, 163–172.
To mate or fight? Male-male competition and alternative mating strategies in Argyrodes antipodiana (Theridiidae, Araneae).CrossRef | 1:STN:280:DC%2BC2cfit1Smsw%3D%3D&md5=9b29f5d5912266c05967c3198465d36eCAS | 24923512PubMed |

Whitehouse, M. (2011). Kleptoparasitic spiders of the subfamily Argyrodinae: a special case of behavioural plasticity. In ‘Spider Behaviour: Flexibility and Versatility’. (Ed. M. E. Herberstein.) (Cambridge University Press: Cambridge.)

Whitehouse, M., Agnarsson, I., Miyashita, T., Smith, D., Cangialosi, K., Masumoto, T., Li, D., and Henaut, Y. (2002). Argyrodes: phylogeny, sociality and interspecific interactions: a report on the Argyrodes symposium, Badplaas 2001. The Journal of Arachnology 30, 238–245.
Argyrodes: phylogeny, sociality and interspecific interactions: a report on the Argyrodes symposium, Badplaas 2001.CrossRef |

Whiting, M. F., Carpenter, J. C., Wheeler, Q. D., and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.
| 1:STN:280:DC%2BD383js1yqtQ%3D%3D&md5=86df74a7ce3b490b4da8ad4ca25d6b71CAS | 11975347PubMed |

Wise, D. H. (1982). Predation by a commensal spider, Argyrodes trigonum, upon its host: an experimental study. The Journal of Arachnology 10, 111–116.

Wunderlich, J. (1988). Die fossilen Spinnen im dominikanischen Bernstein. Beiträge zur Araneologie 2, 1–378.

Wunderlich, J. (2004). Subrecent spiders (Araneae) in copal from Madagascar, with description of new species. Beiträge zur Araneologie 3, 1830–1853.

Wunderlich, J. (2008). On extant and fossil (Eocene) European comb-footed spiders (Araneae: Theridiidae), with notes on their subfamilies, and with descriptions of new taxa. Beiträge zur Araneologie 5, 140–469.

Wunderlich, J. (2011). Some subrecent spiders (Araneae) in copal from Madagascar. Beiträge zur Araneologie 6, 445–460.

Yip, E., Clarke, S., and Rayor, L. (2009). Aliens among us: nestmate recognition in the social huntsman spider, Delena cancerides. Insectes Sociaux 56, 223–231.
Aliens among us: nestmate recognition in the social huntsman spider, Delena cancerides.CrossRef |

Yoshida, H. (2001). The genus Rhomphaea (Araneae: Theridiidae) from Japan, with notes on the subfamily Argyrodinae. Acta Arachnologica 50, 183–192.
The genus Rhomphaea (Araneae: Theridiidae) from Japan, with notes on the subfamily Argyrodinae.CrossRef |

Yoshida, H. (2003). A new genus and three new species of the family Theridiidae (Arachnida: Araneae) from North Borneo. Acta Arachnologica 52, 85–89.
A new genus and three new species of the family Theridiidae (Arachnida: Araneae) from North Borneo.CrossRef |

Zwickl, D. J. (2006). GARLI: genetic algorithm for rapid likelihood inference. Available at http://www.bio.utexas.edu/faculty/antisense/garli/Garli.html [Verified July 2014]



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