Abstract
Understanding the maintenance and evolution of complex group behavioural systems has broad significance to our understanding of social evolution, yet we have little insight into how these systems have evolved. Nest-weaving, a rare group behaviour considered a pinnacle of cooperative action in social insects, involves the coordination of workers and larvae by incorporating larval silk into the nest structure. To investigate the evolution of this complex behaviour in the ant genus Polyrhachis, we used comparative analysis and an inferred molecular phylogeny based on three mitochondrial genes COI, COII and CytB, and three nuclear genes EF1 a-F2, Wg and Tf. Our results showed that arboreality and nest-weaving are closely associated, but in contrast to the previous hypotheses, represent the ancestral state in the monophyletic genus. Nest-weaving within the genus, moreover, is remarkably labile. Arboreality and nest-weaving have been lost and partially regained on at least two occasions: two non-weaving subterranean species (sister taxa likely reflecting a single evolutionary event) have reverted to arboreal nesting habits without regaining the use of silk nests, while a third subterranean species has transitioned to nesting in silk nests on the sides of rocks, obtaining silk from spiders and not their own larvae. The loss of larval cocoons, which is correlated with the most complex form of nest-weaving behavior as typified in Oecophylla, has occurred independently on at least two occasions within Polyrhachis. The repeated loss of nest-weaving behaviour and its partial regaining within the genus provides the first example of a complex group-level trait that did not arise through behavioural progression from simple to complex states. The evolution and loss of complex group-level traits may be more evolutionarily labile than previously appreciated.
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References
Anderson C, Franks NR (2003) Teamwork in animals, robots, and humans. Adv Study Behav 33:1–48
Beckenbach AT, Robson SK, Crozier RH (2005) Single nucleotide +1 frameshifts in an apparently functional mitochondrial cytochrome b gene in ants of the genus Polyrhachis. J Mol Evol 60:141–152
Beekman M, Sumpter DJ, Ratnieks FL (2001) Phase transition between disordered and ordered foraging in Pharaoh’s ants. Proc Natl Acad Sci U S A 98:9703–9706
Bochynek T, Robson SKA (2014) Physical and biological determinants of collective behavioural dynamics in complex systems: Pulling chain formation in the nest-weaving ant Oecophylla smaragdina. PLoS ONE 9:e95112
Bollback J (2006) SIMMAP: Stochastic character mapping of dicrete traits on phylogenies. BMC Bioinforma 7:88
Bolton B (2014) An online catalog of the ants of the world. Available from http://antcat.org. (accessed 15.xi.2014)
Bonabeau E, Theraulaz G, Deneubourg J-LL, Aron S, Camazine S (1997) Self-organization in social insects. Trends Ecol Evol 12:188–193
Bonabeau E, Dorigo M, Theraulaz G (2000) Inspiration for optimization from social insect behaviour. Nature 406:39–42
Brady SG (2003) Evolution of the army ant syndrome: the origin and long-term evolutionary stasis of a complex of behavioral and reproductive adaptations. Proc Natl Acad Sci U S A 100:6575–6579
Britton N, Franks NR, Pratt S, Seeley T (2002) Deciding on a new home: how do honeybees agree? Proc Roy Soc Lond B 269:1383–1388
Burd M, Archer D, Aranwela N, Stradling DJ (2002) Traffic dynamics of the leaf-cuttingant, Atta cephalotes. Am Nat 159:283–293
Camazine S (1991) Self-organizing pattern-formation on the combs of honeybee colonies. Behav Ecol Sociobiol 28:61–76
Ceccarelli FS, Crozier RH (2007) Dynamics of the evolution of Batesian mimicry: molecular phylogenetic analysis of ant-mimicking Myrmarachne (Araneae: Salticidae) species and their ant models. J Evol Biol 20:286–295
Couzin ID (2009) Collective cognition in animal groups. Trends Cogn Sci 13:36–43
Crozier R, Newey PS, Schluns H, Robson SKA (2009) A masterpiece of evolution—Oecophylla weaver ants (Hymenoptera: Formicidae). Myrmecol News 13:57–71
Degnan PH, Lazarus AB, Brock CD, Wernegreen JJ (2004) Host-symbiont stability and fast evolutionary rates in an ant-bacterium association: Cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst Biol 53:95–110
Deneubourg J-LL, Pasteels JM, Verhaeghe J (1983) Probabilistic behaviour in ants: a strategy of errors? J Theor Biol 105:259–271
Deneubourg JL, Goss S, Franks N, Sendova-Franks A, Detrain C, Chrétien L (1991) The dynamics of collective sorting: Robot-like ants and ant-like robots. In: Meyer JA, Wilson EO (eds) Simulations of animal behavior: from animals to animals. Cambridge University Press, Cambridge, pp 356–365
Dorigo M, Stützle T (2004) Ant colony optimization. The MIT Press, Cambride
Dornhaus A, Powell S, Bengston S (2012) Group size and its effects on collective organization. Annu Rev Entomol 57:123–141
Dorow WHO (1995) Revision of the ant genus Polyrhachis Smith, 1857 (Hymenoptera: Formicidae: Formicinae) on subgenus level with keys, checklist of species and bibliography. Cour Forschungsinst Senckenb 185:1–113
Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2012) Geneious v5.6. In, http://www.geneious.com
Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Ann Rev Ecol Evol Syst 42:91–110
Dussutour A, Fourcassié V, Helbing D, Deneubourg JL (2004) Optimal traffic organization in ants under crowded conditions. Nature 428:70–73
Franks NR, Sendova-Franks AB (1992) Brood sorting by ants: Distributing the workload over the work-surface. Behav Ecol Sociobiol 30:109–123
Franks NR, Pratt S, Mallon E, Britton N, Sumpter DJT (2002) Information flow, opinion polling and collective intelligence in house-hunting social insects. Phil Trans Roy Soc Lond B 357:1567–1583
Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124
Halloy J, Sempo G, Caprari G, Rivault C, Asadpour M, Tache F, Said I, Durier V, Canonge S, Ame JM, Detrain C, Correll N, Martinoli A, Mondada F, Siegwart R, Deneubourg J-LL (2007) Social integration of robots into groups of cockroaches to control self-organized choices. Science 318:1155–1158
Hölldobler B, Wilson EO (1977) Weaver ants. Sci Am 237:146–154
Holldobler B, Wilson EO (1983) The evolution of communal nest-weaving in ants. Amer Sci 71:490–499
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge
Hölldobler B, Obermayer M, Plowes NJR, Fisher BL (2014) New exocrine glands in ants: the hypostomal gland and basitarsal gland in the genus Melissotarsus (Hymenoptera: Formicidae). Naturwiss 101:527–532
Huelsenbeck J, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755
Huelsenbeck J, Nielsen R, Bollback J (2003) Stochastic mapping of morphological characters. Syst Biol 52:131–158
Hung A (1967) A revision of the ant genus Polyrhachis at the subgeneric level (Hymenoptera: Formicidae). Trans Amer Ent Soc 93:395–422
Jeanne RL (1975) The adaptiveness of social wasp nest architecture. Q Rev Biol 50:267–287
Johnson BR, Lam SK (2010) Self-organization, natural selection, and evolution: Cellular hardware and genetic software. Bioscience 60:879–885
Johnson RN, Agapow P-M, Crozier RH (2003) A tree island approach to inferring phylogeny in the ant subfamily Formicinae, with especial reference to the evolution of weaving. Mol Phylogenet Evol 29:317–330
Karsai I, Penzes Z (1998) Nest shapes in paper wasps: can the variability of forms be deduced from the same construction algorithm? Proc Roy Soc Lond B 265:1261–1268
Kohout RJ (2006) Review of Polyrhachis (Cyrtomyrma) Forel (Hymenoptera: Formicidae: Formicinae) of Australia, Borneo, New Guinea and the Solomon islands with descriptions of new species. Mem Qld Mus 52:87–146
Kohout RJ (2010) A review of the Australian Polyrhachis ants of the subgenera Myrmhopla Forel and Hirtomyrma subgen. Nov. (Hymenoptera: Formicidae: Formicinae). Mem Qld Mus 55:167–204
Kohout RJ (2013) Revision of Polyrhachis (Hagiomyrma) Wheeler, 1911 (Insecta: Hymenoptera: Formicidae: Formicinae). Mem Qld Mus 56:487–577
Kronauer DJ, Schoning C, Vilhelmsen LB, Boomsma JJ (2007) A molecular phylogeny of Dorylus army ants provides evidence for multiple evolutionary transitions in foraging niche. BMC Evol Biol 7:56
Larget B, Simon D (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759
Lioni A, Deneubourg J-LL (2004) Collective decision through self-assembling. Naturwiss 91:237–241
Lioni A, Sauwens C, Theraulaz G, Deneubourg JL (2001) Chain formation in Oecophylla longinoda. J Insect Behav 14:679–696
Lucky A, Trautwein MD, Guénard BS, Weiser MD, Dunn RR (2012) Tracing the rise of ants—Out of the ground. PloS ONE 8:e84012
Maddison W, Maddison D (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. In, http://mesquiteproject.org
Miller M, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogentic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, LA pp 1 - 8., New Orleans,, pp 1-8
Moreau CS (2008) Unraveling the evolutionary history of the hyperdiverse ant genus Pheidole (Hymenoptera: Formicidae). Mol Phylogenet Evol 48:224–239
Moreau CS, Bell CD (2013) Testing the museum versus cradle tropical biological diversity hypothesis: Phylogeny, diversification, and ancestral biogeographic range evolution of the ants. Evolution 67:2240–2257
Page RE, Mitchell SD (1998) Self-organization and the evolution of division of labor. Apidologie 29:171–190
Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc Roy Soc London B 255:37–45
Pagel M (1999) The maximum likelihood approach to reconstructing ancestral character states of dicrete characters on phylogenies. Syst Biol 48:612–622
Posada D, Crandall K (2001) Selecting the best-fit model of nucleotide substitution. Syst Biol 50:580–601
Poulsen M, Boomsma JJ (2005) Mutualistic fungi control crop diversity in fungus-growing ants. Science 307:741–744
Powell S, Franks NR (2006) Ecology and the evolution of worker morphological diversity: a comparative analysis with Eciton army ants. Func Ecol 20:1105–1114
Pratt S, Mallon E, Sumpter D, Franks N (2002) Quorum sensing, recruitment, and collective decision-making during colony emigration by the ant Leptothorax albipennis. Behav Ecol Sociobiol 52:117–127
Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311
Reid CR, Sumpter DJT, Beekman M (2011) Optimisation in a natural system: Argentine ants solve the towers of Hanoi. J Exp Biol 214:50–58
Richardson RC (2001) Complexity, self-organization and selection. Biol Philos 16:653–682
Robson SKA, Kohout RJ (2005) Evolution of nest-weaving behaviour in arboreal nesting ants of the genus Polyrhachis Fr. Smith (Hymenoptera: Formicidae). Aust J Entomol 44:164–169
Robson SKA, Kohout RJ (2007) A review of the nesting habits and socioecology of the ant genus Polyrhachis Fr. Smith. Asian Myrmecol 1:81–99
Robson SK, Traniello JFA (1998) Resource assessment, recruitment behavior, and organization of cooperative prey retrieval in the ant Formica schaufussi (Hymenoptera: Formicidae). J Insect Behav 11:1–22
Robson S, Traniello J (1999) Key individuals and the organisation of labour in ants. In:Detrain C, Pasteels J, Deneubourg J (eds) Information Processing in Social Insects. Verlag Press, pp 239-259
Robson S, Traniello J (2002) Transient division of labor and behavioral specialization in the ant Formica schaufussi. Naturwiss 89:128–131
Schlüns E (2011) Molecular ecology and phylogenetics in Formicine ants. PhD thesis, James Cook University:1-109
Schluter D, Price T, Mooers A, Ludwig D (1997) Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–1711
Schockaert S, De Cock M, Cornelis C, Kerre E (2007) Clustering web search results using fuzzy ants. Int J Intel Syst 22:455–474
Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci U S A 105:5435–5440
Seeley TD (2002) When is self-organization used in biological systems? Biol Bull 202:314–318
Seeley TD, Visscher PK (2004) Quorum sensing during nest-site selection by honeybee swarms. Behav Ecol Sociobiol 56:594–601
Sumpter DJ (2006) The principles of collective animal behaviour. Phil Trans Roy Soc Lond B 361:5–22
Traniello J, Robson SKA (1995) Trail and teritorial communication in social insects. In, Chemical Ecology of Insects II (RT Carde, WJ Bell):241–286
Ward PS, Brady SG, Fisher BL, Schultz TR (2010) Phylogeny and biogeography of dolichoderine ants: Effects of data partitioning and relict taxa on historical inference. Syst Biol 59:342–362
Acknowledgments
This research is dedicated to the late Ross H. Crozier, for his significant contributions to the study of social evolution in general and Polyrhachis in particular. We thank C. Crozier, A.J. Shuetrim, E.A. Schlüns, M. Guzik and M. Henshaw for their laboratory assistance, Seki Yamane, Peter Dwyer and Monica Minnegal for samples, and the Australian Research Council Discovery Grant DP1093553 and Centre for Tropical Biodiversity & Climate Change Research Grant Scheme for financial support. Many thanks to Antweb.org and B.L. Fisher for use of the photographs of Polyrhachis.
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Robson, S.K.A., Kohout, R.J., Beckenbach, A.T. et al. Evolutionary transitions of complex labile traits: Silk weaving and arboreal nesting in Polyrhachis ants. Behav Ecol Sociobiol 69, 449–458 (2015). https://doi.org/10.1007/s00265-014-1857-x
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DOI: https://doi.org/10.1007/s00265-014-1857-x