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Army Ants Colony Fusion and Worker Reproduction After Queen Loss In Downloaded from rspb.royalsocietypublishing.org on February 19, 2010 Colony fusion and worker reproduction after queen loss in army ants Daniel J. C. Kronauer, Caspar Schöning, Patrizia d'Ettorre and Jacobus J. Boomsma Proc. R. Soc. B 2010 277, 755-763 first published online 4 November 2009 doi: 10.1098/rspb.2009.1591 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2009/10/29/rspb.2009.1591.DC1.h tml References This article cites 49 articles, 3 of which can be accessed free http://rspb.royalsocietypublishing.org/content/277/1682/755.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections behaviour (1065 articles) ecology (1202 articles) evolution (1430 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rspb.royalsocietypublishing.org on February 19, 2010 Proc. R. Soc. B (2010) 277, 755–763 doi:10.1098/rspb.2009.1591 Published online 4 November 2009 Colony fusion and worker reproduction after queen loss in army ants Daniel J. C. Kronauer*,†, Caspar Scho¨ning‡, Patrizia d’Ettorre and Jacobus J. Boomsma Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enig- matic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male pro- duction by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable. Keywords: altruism; army ant; Dorylus; inclusive fitness; queen death; worker reproduction 1. INTRODUCTION Analogously to immune systems, social insects therefore How evolution by natural selection can produce altruists, use nest-mate recognition cues that allow them to dis- individuals that help others at an overall cost to their own criminate between self (individuals belonging to their fitness, remains one of the central problems in evolution- own colony) and non-self (individuals belonging to ary biology. Following Hamilton’s (1964) seminal paper, foreign colonies). These cues are mainly expressed as a an immense research effort has been devoted to solving blend of hydrocarbons on the cuticle, and form a this puzzle, which has produced the consensus that phe- colony-specific Gestalt odour (Vander Meer & Morel notypic altruism can only evolve and be evolutionarily 1998; Lenoir et al. 1999). stable if the behaviour is preferentially directed towards The few known cases where social insect workers individuals that carry identical alleles, either by actively join foreign colonies are therefore highly intriguing. common descent or by explicit recognition (‘green The vast supercolonies of some invasive ants are one beards’) (Lehmann & Keller 2006). example where workers are not related and freely move The best known examples of altruism are colonies of euso- between nests without being attacked. While their native cial insects in which workers forage and care for the brood of counterparts have genetically structured populations, it their mother queens. The most complex insect societies are has been argued that invasive supercolonies might not be highly integrated entities that have been described as stable over evolutionary time because kin selection can ‘superorganisms’ (Wheeler 1911; Ho¨lldobler & Wilson no longer act on worker traits (see Helantera¨ et al. 2009). Similar to conventional organisms, they have 2009 for a recent review). A second example is social evolved mechanisms to maintain their colony integrity insect workers that drift into foreign colonies and are and to guard themselves against intrusion and exploita- apparently able to evade host colony recognition systems. tion by unrelated individuals from outside (Wheeler Although the occasional drifter could merely be a conse- 1911; Ho¨lldobler & Wilson 2009). Because of kinship quence of individual navigation and recognition errors, ties, a social insect worker would normally maximize recent work has shown that nest drifting can often be inclusive fitness by remaining in her natal colony, rather understood as a form of social parasitism rather than altru- than helping unrelated individuals in other nests. ism (see Beekman & Oldroyd 2008 for a recent review). Drifting is also adaptive in the paper wasp Polistes canadensis, but here fitness rewards are indirect, because populations * Author for correspondence ([email protected]). are viscous and drifters end up in nests to which they are † Present address: Museum of Comparative Zoology, Harvard related (Sumner et al. 2007). University, 26 Oxford Street, Cambridge, MA 02138, USA. ‡ Present address: La¨nderinstitut fu¨r Bienenkunde, Friedrich- Fusions between the huge societies of army ants after Engels-Strasse 32, 16540 Hohen Neuendorf, Germany. queen loss potentially constitute a third striking example Electronic supplementary material is available at http://dx.doi.org/10. of workers actively joining foreign colonies. However, 1098/rspb.2009.1591 or via http://rspb.royalsocietypublishing.org. the sporadic accounts are largely anecdotal and only Received 3 September 2009 Accepted 14 October 2009 755 This journal is q 2009 The Royal Society Downloaded from rspb.royalsocietypublishing.org on February 19, 2010 756 D. J. C. Kronauer et al. Colony fusion in army ants concern the neotropical genus Eciton. Schneirla (1949) removal, orphaned colonies were checked daily for foraging and Schneirla & Brown (1950) reported that while trails, emigrations, the production of males or colony fusions, intact colonies of E. burchellii and E. hamatum never without further disturbing them. After a colony fusion was mingle when they meet during swarm raids or emigra- suspected, the nest was opened and a sample of workers and tions, workers of queenless colonies actively trace and brood was taken for genetic and cuticular chemistry analysis. sometimes join foreign conspecific colonies. Schneirla Voucher specimens from this population have been deposited (1971) hypothesized that the loss of the queen was in the entomology collection of the Zoological Museum quickly followed by pronounced changes in the colony Copenhagen (Kronauer et al.2006). Gestalt odour, which should weaken nest-mate recog- Two legs of the captured queens were removed and stored nition and ultimately allow colonies to merge without for genetic analyses. The queens’ head and thorax were aggression. This might be a plausible proximate expla- washed in 900 ml pentane as described below for workers to nation because ant queens can contribute substantially study their cuticular hydrocarbons (CHCs). In a subset of to the colony Gestalt odour (Breed & Bennett 1987), colonies, three to five workers were collected for genetic and but it does not offer an ultimate explanation for why chemical analyses immediately before queen removal, one day colony fusions have evolved. after queen removal, and subsequently once a week until the Assuming that merging colonies are unrelated, Lin & colony merged or died/disappeared. If a colony fusion was sus- Michener (1972) viewed colony fusions in army ants as pected, 10 workers were collected from the putatively mixed direct evidence against inclusive fitness effects being a colony. For all individuals whose cuticular profiles were ana- major driver for the evolution of social behaviour and con- lysed, we removed the left hind leg and stored it for genetic cluded that, by merging with foreign colonies after queen analyses to allow assignment of workers to one of two parental loss, ‘they (army ants) cannot benefit their own genotype, colonies in recently merged nests. To extract CHCs, each but instead benefit a competing one’ (Lin & Michener worker was washed in 300 ml pentane (HPLC grade, Sigma- 1972). Bourke & Franks (1995) agreed that fusing army Aldrich) for 10 min, after which the solvent was allowed to ant colonies are probably not closely related because evaporate and the extract stored for later analysis. their nomadic lifestyle will lead to the dispersal of daughter Because colony emigrations of D. molestus are partly sub- colonies. Assuming that queenless workers have no alterna- terranean and not easy
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