Wingless Virgin Queens Assume Helper Roles in Acromyrmex Leaf-Cutting Ants
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Magazine R671 animal associations. The technology is plasticity for adopting specific suitable for long-term deployment on Wingless virgin behaviours depending on their age relatively small animals, and overcomes queens assume and the needs of the colony [6], key constraints of other data-collection but their reproductive potential is methods. Importantly, with its high helper roles in always permanently reduced. The sampling rates and excellent tag-to- behavioural repertoires of queens tag detection range, Encounternet can Acromyrmex tend to be limited to mating, colony generate time-resolved association data leaf-cutting ants founding and egg-laying, and needed to link network topologies to this never changes in response biological processes — a key challenge to queen condition. This should in social network analyses [2,3]. Volker Nehring1,2,*, imply that gynes — unmated virgin Jacobus J. Boomsma1, queens —should be cannibalized Supplemental Information and Patrizia d’Ettorre1,3 or otherwise disposed of when Supplemental information including experi- they somehow fail to disperse on mental procedures and two figures can be Division of labour is the hallmark a mating flight, similar to infertile found with this article online at of advanced societies, because diploid males [7,8]. Uselessness for http://dx.doi.org/10.1016/j.cub.2012.06.037. specialization carries major both colony-founding and altruistic efficiency benefits in spite of behaviour means that failed queens Competing Interests Encounternet was conceived and developed costs owing to reduced individual have zero fitness and might thus at the University of Washington, Seattle, USA, flexibility [1]. The trade-off between be even expected to die voluntarily, and BO, JBu and JBo are currently working efficiency and flexibility is expressed as recycling of their tissues and on the technology’s commercial exploitation. throughout the social insects, where prevention of further consumption facultative social species have small of scarce resources will offer them Acknowledgments colonies and reversible caste roles at least some indirect fitness when We thank C. Lambert, T. Mennesson and and advanced eusocial species their resources will benefit properly J.-E. Lombardet for facilitating field logistics, have permanently fixed queen and endowed siblings. C. Anagnostou for field assistance, W. Loo worker castes. This usually implies We observed field colonies of for help with R-code, R.C. Fleischer for that queens irreversibly specialize the leaf-cutting ants Acromyrmex molecular sexing, the BBSRC for funding on reproductive tasks [2]. Here, we echinatior and A. octospinosus that (grant BB/G023913/1 to CR), and the report an exception to this rule by contained several non-inseminated Province Sud and SEM Mwe Ara for generous showing that virgin queens (gynes) wingless gynes besides the mother support in New Caledonia. of the advanced eusocial leaf-cutting queen (Supplemental Information ant Acromyrmex echinatior switch published with this article online). References 1. Krause, J., and Ruxton, G.D. (2002). Living in to carrying out worker tasks such as As these queens had been allowed Groups (Oxford: Oxford Univ. Press). brood care and colony defence when to live, we hypothesized that they 2. Whitehead, H. (2008). Analyzing Animal they fail to mate and disperse. These might still be worth their keep if Societies (Chicago: Chicago Univ. Press). 3. Croft, D.P., James, R., and Krause, J. (2008). behaviours allow them to obtain they would assume helper roles that Exploring Animal Social Networks (Princeton: indirect fitness benefits (through were of value for their colony. To test Princeton Univ. Press). 4. Rutz, C., and Hays, G.C. (2009). New frontiers assisting the reproduction of their this hypothesis, we experimentally in biologging science. Biol. Lett. 5, 289–292. mother) after their direct fitness removed the wings of normal 5. Hunt, G.R. (1996). Manufacture and use of options (their own reproduction) gynes and quantified worker-like hook-tools by New Caledonian crows. Nature 379, 249–251. have become moot. We hypothesize behaviours. As controls, we used 6. Hunt, G.R., and Gray, R.D. (2003). that this flexibility could (re-)evolve both completely un-manipulated Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc. secondarily because these ants only gynes, and gynes with one middle R. Soc. B 270, 867–874. feed on fungal mycelium and thus leg removed. This mutilation was not 7. Rutz, C., Bluff, L.A., Weir, A.A.S., and Kacelnik, could not benefit from cannibalising expected to affect normal behaviour A. (2007). Video cameras on wild birds. Science 318, 765. redundant gynes, and because as queens missing a leg are 8. Laland, K.N. (2008). Animal cultures. Curr. Biol. queens have retained behavioural occasionally observed as functional 18, R366–R370. 9. Holzhaider, J.C., Sibley, M.D., Taylor, A.H., repertoires for foraging, nursing, colony mothers. Singh, P.J., Gray, R.D., and Hunt, G.R. (2011). and defense, which they naturally Acromyrmex gynes with their The social structure of New Caledonian crows. express during colony founding. wings experimentally removed were Anim. Behav. 81, 83–92. 10. Whitehead, H., and Lusseau, D. (2012). Animal Permanence of caste is the most more likely to conduct worker tasks: social networks as substrate for cultural fundamental difference between unlike the control gynes, they took behavioural diversity. J. Theor. Biol. 294, 19–28. eusocial and cooperative breeding care of brood that we introduced 1Department of Zoology, University of Oxford, [2]. Helpers of the latter category into experimental nests (Figure 1A,B) South Parks Road, Oxford OX1 3PS, UK. may become breeders later in and they attacked non-nestmates 2Present address: School of Biology, University life and thus retain full flexibility (Figure 1C). A second nestmate of St Andrews, St Andrews KY16 9TH, UK. towards the eventual pursuit of recognition experiment, in which 3Department of Physics, University of Bath, direct fitness. Illustrative examples tethered gynes were presented with 4 Bath BA2 7AY, UK. School of Biological are cooperatively breeding birds, nestmate or non-nestmate odour, Sciences, University of Auckland, PB 92019, Auckland 1142, NZ. 5Department of Electrical paper wasps and some Ponerinae showed that both the control and Engineering, University of Washington, Seattle, ants [3–5]. Workers of eusocial wingless gynes were equally able to WA 98195-3770, USA. ants and honeybees, by contrast, discriminate between nestmate and *E-mail: [email protected] at best retain some phenotypic non-nestmate cues (Figure 1D). Current Biology Vol 22 No 17 R672 is not an oversight by generations of natural historians, but that there are likely to be two selection forces that make working/defending gynes particularly probable in fungus- growing ants such as Acromyrmex. First, Acromyrmex queens are semiclaustral, which means that they forage during colony founding, unlike the claustral queens of most ants that seal their founding burrow to live on body reserves until their first workers hatch [9]. Acromyrmex gynes have thus retained a working and defending repertoire that becomes temporarily expressed in response to dispersal and insemination, so could easily be co-opted. Second, attine ants consume almost exclusively fungal tissue, and are thus likely to have lost the ability to digest animal tissue. Acromyrmex fungus-gardens have also never been observed to contain parts of dead insects as substrate in any appreciable amount [10]. This means that workers cannot recoup investments that went into raising reproductives, so they may as well let wingless gynes serve the colony while living on the fat and carbohydrate reserves that Figure 1. Virgin queens (gynes) as helpers in Acromyrmex leaf-cutting ants. were deposited to prepare them Wingless Acromyrmex gynes carry out worker behaviour in contrast to winged control gynes for founding a new colony. This (leg-mutilated and un-manipulated). (A and B) They transported brood items back to their would imply that wingless gynes fungus garden (three colonies tested) and (C) attacked non-nestmate intruders, while control expressing worker behaviour are gynes rarely engaged in these behaviours (boxplots show interquartile ranges and medians; not expected to be fed, because whiskers cover all data points; four colonies tested in the field and laboratory, see also Figure their existence only makes sense S1). Gynes hardly ever attacked nestmates (p < 0.001, interaction gyne type x intruder p < 0.001). (D) Tethered wingless gynes and control gynes were all able to discriminate non-nest- when their siblings profit at no mates from nestmates: all three types of gynes were more prone to opening their mandibles cost. However, our current set-up (showing threat) when confronted with non-nestmate than with nestmate odour or solvent (p < did not allow us to investigate this 0.05, three colonies). Wingless gynes were generally more likely to open their mandibles than possibility. other gynes (p < 0.05), consistent with expression of more aggressive behaviour; the ability to We hypothesize that the same discriminate between nestmate and non-nestmate odours was, however, similar for all gynes logic may apply in other attine ants (interaction odour x gyne type p > 0.05). Sample sizes are indicated above the bars and boxes (*** p < 0.001, * p < 0.05, n.s. p > 0.05). and that soldier/nurse gynes might occur also in