Abstract
Cooperation and group living often evolves through kin selection. However, associations between unrelated organisms, such as different species, can evolve if both parties benefit from the interaction. Group living is rare in spiders, but occurs in cooperative, permanently social spiders, as well as in territorial, colonial spiders. Mixed species spider colonies, involving closely related species, have rarely been documented. We examined social interactions in newly discovered mixed-species colonies of theridiid spiders on Bali, Indonesia. Our aim was to test the degree of intra- and interspecific tolerance, aggression and cooperation through behavioural experiments and examine the potential for adoption of foreign brood. Morphological and genetic analyses confirmed that colonies consisted of two related species Chikunia nigra (O.P. Cambridge, 1880) new combination (previously Chrysso nigra) and a yet undescribed Chikunia sp. Females defended territories and did not engage in cooperative prey capture, but interestingly, both species seemed to provide extended maternal care of young and indiscriminate care for foreign brood. Future studies may reveal whether these species adopt only intra-specific young, or also inter-specifically. We classify both Chikunia species subsocial and intra- and interspecifically colonial, and discuss the evolutionary significance of a system where one or both species may potentially benefit from mutual tolerance and brood adoption.
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References
Agnarsson I (2004) Morphological phylogeny of cobweb spiders and their relatives (Araneae, Araneoidea, Theridiidae). Zool J Linnean Soc 141(4):447–626
Agnarsson I (2006) A revision of the New World eximius lineage of Anelosimus (Araneae, Theridiidae) and a phylogenetic analysis using worldwide exemplars. Zool J Linnean Soc 146(4):453–593
Agnarsson I (2010) The utility of ITS2 in spider phylogenetics: notes on prior work and an example from Anelosimus. J Arachnol 38(2):377–382
Agnarsson I (2012) A new phylogeny of Anelosimus and the placement and behavior of Anelosimus vierae n. sp from Uruguay (Araneae: Theridiidae). J Arachnol 40(1):78–84
Agnarsson I, Aviles L, Coddington JA, Maddison WP (2006) Sociality in theridiid spiders: repeated origins of an evolutionary dead end. Evolution 60(11):2342–2351
Agnarsson I, Maddison WP, Aviles L (2007) The phylogeny of the social Anelosimus spiders (Araneae: Theridiidae) inferred from six molecular loci and morphology. Mol Phylogenet Evol 43(3):833–851
Arnedo MA, Hormiga G, Scharff N (2009) Higher-level phylogenetics of linyphiid spiders (Araneae, Linyphiidae) based on morphological and molecular evidence. Cladistics 25(3):231–262
Avilés L (1997) Causes and consequences of cooperation and permanent-sociality in spiders. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 476–498
Aviles L, Maddison W (1991) When is the sex-ratio biased in social spiders?: chromosome studies of embryos and male meiosis in Anelosimus species (Araneae, Theridiidae). J Arachnol 19(2):126–135
Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes, http://CRAN.R-project.org/package=lme4
Beavis AS, Rowell DM, Evans T (2007) Cannibalism and kin recognition in Delena cancerides (Araneae: Sparassidae), a social huntsman spider. J Zool 271(2):233–237
Bilde T, Lubin Y (2011) Group living in spiders: cooperative breeding and coloniality. In: Herberstein ME (ed) Spider behaviour, flexibility and versatility. Cambridge University Press, New York
Bilde T, Lubin Y, Smith D, Schneider JM, Maklakov AA (2005) The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor. Evolution 59(1):160–174
Boomsma JJ (2009) Lifetime monogamy and the evolution of eusociality. Philos Trans R Soc B Biol Sci 364(1533):3191–3207
Boucher DH, James S, Keeler KH (1982) The Ecology of Mutualism. Annu Rev Ecol Syst 13:315–347
Buschinger A (1986) Evolution of Social Parasitism in Ants. Trends Ecol Evol 1(6):155–160
Deeleman-Reinhold CL (2009) Spiny theridiids in the Asian tropics. Systematics, notes on behaviour and species richness (Araneae: Theridiidae: Chrysso, Meotipa). Contrib Nat Hist 12:403–436
R Development Core Team (2011) R: A language and environment for statistical computing, http://www.R-project.org/R Foundation for Statistical Computing. Vienna, Austria
Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci U S A 95(15):8676–8680
Eberhard WG, Agnarsson I, Levi HW (2008) Web forms and the phylogeny and theridiid spiders (Araneae: Theridiidae): chaos from order. Syst Biodivers 6(4):415–475
Elgar MA (1994) Experimental evidence of a mutualistic association between 2 web-building spiders. J Anim Ecol 63(4):880–886
Foelix RF (1996) Biology of spiders. Oxford University Press, Oxford
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Furey FE (1998) Two cooperatively social populations of the theridiid spider Anelosimus studiosus in a temperate region. Anim Behav 55:727–735
Green P (1999) PHRAP, http://phrap.org/
Green P, Ewing B (2002). PHRED, http://phrap.org/
Grostal P, Walter DE (1997) Kleptoparasites or commensals? Effects of Argyrodes antipodianus (Araneae: Theridiidae) on Nephila plumipes (Araneae: Tetragnathidae). Oecologia 111(4):570–574
Hamilton WD (1964) Genetical evolution of social behaviour I. J Theor Biol 7(1):1–16
Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc London, Ser B 270:S96–S99
Hedin MC, Maddison WP (2001) A combined molecular approach to phylogeny of the lumping spider subfamily Dendryphantinae (Araneae: Salticidae). Mol Phylogenet Evol 18(3):386–403
Hodge MA, Uetz GW (1996) Foraging advantages of mixed-species association between solitary and colonial orb-weaving spiders. Oecologia 107(4):578–587
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755
Jackson RR (1986) Communal jumping spiders (Araneae, Salticidae) from Kenya—interspecific nest complexes, cohabitation with web-building spiders, and intraspecific interactions. N Z J Zool 13(1):13–26
Jackson RR, Nelson XJ, Salm K (2008) The natural history of Myrmarachne melanotarsa, a social ant-mimicking jumping spider. N Z J Zool 35(3):225–235
Johannesen J, Lubin Y, Smith DR, Bilde T, Schneider JM (2007) The age and evolution of sociality in Stegodyphus spiders: a molecular phylogenetic perspective. Proc R Soc Lond B Biol 274(1607):231–237
Jones TC, Riechert SE, Dalrymple SE, Parker PG (2007) Fostering model explains variation in levels of sociality in a spider system. Anim Behav 73:195–204
Kullmann EJ (1972) Evolution of social behavior in spiders (Araneae - Eresidae and Theridiidae). Am Zool 12(3):419–426
Lubin Y, Bilde T (2007) The evolution of sociality in spiders. Adv Study Behav 37:83–145
Maddison D, Maddison W (2011a) Chromaseq: a Mesquite module for analyzing sequence chromatograms. Version 0.99, http://mesquiteproject.org/packages/chromaseq
Maddison W, Maddison D (2011b) Mesquite: a modular system for evolutionary analysis. Version 2.75, http://mesquiteproject.org
Menzel F, Bluthgen N (2010) Parabiotic associations between tropical ants: equal partnership or parasitic exploitation? J Anim Ecol 79(1):71–81
Peres CA (1992) Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and Saguinus mystax. Behav Ecol Sociobiol 31(5):339–347
Peres CA (1993) Anti-predation benefits in a mixed-species group of Amazonian tamarins. Folia Primatol 61(2):61–76
PlateauxQuenu C, Horel A, Roland C (1997) A reflection on social evolution in two different groups of arthropods: halictine bees (Hymenoptera) and spiders (Arachnida). Ethol Ecol Evol 9(2):183–196
Platnick NI (2012) The World Spider Catalog, Version 12.5, http://research.amnh.org/iz/spiders/catalog American Museum of Natural History
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256
Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53(5):793–808
Rothstein SI, Robinson SK (1998) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, New York
Schneider JM (2002) Reproductive state and care giving in Stegodyphus (Araneae: Eresidae) and the implications for the evolution of sociality. Anim Behav 63:649–658
Schneider JM, Bilde T (2008) Benefits of cooperation with genetic kin in a subsocial spider. Proc Natl Acad Sci U S A 105(31):10843–10846
Sebastian PA, Peter KV (2009) Spiders of India. Universities Press (India), Hyderabad
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680
Uetz GW (1989) The Ricochet effect and prey capture in colonial spiders. Oecologia 81(2):154–159
Uetz GW, Hieber CS (1997) Colonial web-building spiders: balancing costs and benefits of group-living. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 458–475
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc., San Diego, pp 315–322
Whiting MF, Carpenter JC, Wheeler QD, Wheeler WC (1997) The strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol 46(1):1–68
Acknowledgments
We would like to thank Maurice Leponce for sharing his discovery of the spider colonies with us, and Léon Baert for preliminary species identification. Thanks to Yael Lubin and all members of the Spider Lab at Aarhus University for the useful comments to a previous version of this manuscript. This study was supported by the Danish Research Council FNU 495997 and by the National Science Foundation DEB-1050187-1050253.
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Communicated by: Sven Thatje
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Grinsted, L., Agnarsson, I. & Bilde, T. Subsocial behaviour and brood adoption in mixed-species colonies of two theridiid spiders. Naturwissenschaften 99, 1021–1030 (2012). https://doi.org/10.1007/s00114-012-0983-4
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DOI: https://doi.org/10.1007/s00114-012-0983-4