In human society selfish use of common resources

can lead to disaster, a situation known as the ‘tragedy

of the commons’ (TOC). Although a TOC is

usually prevented by coercion, theory predicts that

close kinship ties can also favour reduced exploitation.

We test this prediction using data on a TOC

occurring in Melipona bee societies

Ratnieks, F.L.W.

Wenseleers, T.

English

PubMed

In human society selfish use of common resources can lead to disaster, a situation known as the 'tragedy of the commons' (TOC). Although a TOC is usually prevented by coercion, theory predicts that close kinship ties can also favour reduced exploitation. We test this prediction using data on a TOC occurring in Melipona bee societies.status: Publishe

Wenseleers, Tom

Ratnieks, Francis L.W.

Lirias

Tragedy of the commons in Melipona bees

White Rose Research Online

This is a repository copy of Tragedy of the commons in Melipona bees .White Rose Research Online URL for this paper:http://eprints.whiterose.ac.uk/301/Article:Wenseleers, T. and Ratnieks, F.L.W. (2004) Tragedy of the commons in Melipona bees. Proceedings of the Royal Society Series B: Biological Sciences, 271 (1 (Sup). S310-S312.ISSN 0962-8452 https://doi.org/10.1098/rsbl.2003.0159eprints@whiterose.ac.ukhttps://eprints.whiterose.ac.uk/Reuse Unless indicated otherwise, fulltext items are protected by copyright with all rights reserved. The copyright exception in section 29 of the Copyright, Designs and Patents Act 1988 allows the making of a single copy solely for the purpose of non-commercial research or private study within the limits of fair dealing. The publisher or other rights-holder may allow further reproduction and re-use of this version - refer to the White Rose Research Online record for this item. Where records identify the publisher as the copyright holder, users can verify any specific terms of use on the publisher’s website. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing eprints@whiterose.ac.uk including the URL of the record and the reason for the withdrawal request. Tragedy of the commonsin Melipona beesTom Wenseleers* and Francis L. W. RatnieksLaboratory of Apiculture and Social Insects, Department of Animaland Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK*Author and address for correspondence: Laboratory of Entomology,University of Leuven, Naamestraat 59, B-3000 Leuven, Belgium(tom.wenseleers@bio.kuleuven.ac.be).Recd 05.11.03; Accptd 22.12.03; Published online 03.03.04In human society self ish use of common resourcescan lead to disaster, a situation known as the ‘tra-gedy of the commons’ (TOC). Although a TOC isusually prevented by coercion, theory predicts thatclose kinship ties can also favour reduced exploi-tation. We test this prediction using data on a TOCoccurring in Melipona bee societies.Keywords: caste conflict; tragedy of the commons;stingless bees; Melipona1. INTRODUCTIONSince influential analysis by Hardin (1968) of the ‘tragedyof the commons’ (TOC), the consensus has been thatcoercive management is necessary to prevent overexploit-ation of common resources such as fish stocks or grazingland (Hardin 1998; Ostrom 1999). Hardin (1968) arguedthat rational individuals benefit from increasing theirshare, even if this depletes the resource on which theydepend. In his view, the only way to curb individual self-ishness and prevent a TOC was by ‘mutual coercionmutually agreed upon’ (Hardin 1968). Models developedby evolutionary theorists (Hamilton 1964; Frank 1995,1998), however, show an additional mechanism. If thelevel of exploitation is heritable and groups are composedof kin, a rational or ‘evolutionary stable’ exploitation ratewill evolve that is inversely related to genetic relatedness(Frank 1995, 1998). However, this prediction has neverbeen tested because in most societies or family groups kin-ship benefits co-occur with coercion (Mock & Parker1998), making it impossible to determine their relativecontributions. We test the effects of kinship on the out-come of a TOC that, uniquely, cannot be prevented bycoercion. It concerns the exploitation of a commonresource—the workforce—in Melipona stingless beesocieties.In highly eusocial bees, such as honeybees and stinglessbees, all work is carried out by morphologically specializedworker individuals that, like queens, are female (Wilson1971). The workforce is necessary for colony repro-duction, whether by rearing males or by establishing newcolonies via colony fission, in which a queen and a swarmof workers establish a new nest. Becoming a queen, how-ever, is potentially more rewarding than becoming aworker since queens have greater reproductive potentialthan workers and only queens can ever head daughter col-onies (Bourke & Ratnieks 1999; Wenseleers et al. 2003).So why do more females not attempt to develop as queensrather than workers? In TOC terms, what prevents theProc. R. Soc. Lond. B (Suppl.) 271, S310–S312 (2004) S310  2004 The Royal SocietyDOI 10.1098/rsbl.2003.0159common resource—the workforce—from being exploitedby larvae selfishly choosing to develop into queens? As inHardin’s ‘mutual coercion mutually agreed upon’, a TOCis usually prevented by enforcement (Bourke & Ratnieks1999). In honeybees (Apis) and most stingless bees(Trigonini), queens are larger than workers (Wilson1971). As a result, the adult workers can prevent larvalfemales from developing into queens by controlling theiraccess to food (‘nutritional caste determination’; figure 1).As expected from theory, colonies in these taxa rear fewqueens, just enough to permit seasonal swarming or super-sedure of a failing mother queen (Wenseleers et al. 2003).For example, in the honeybee Apis mellifera and in thetrigonine bee Tetragonisca angustula, only ca. 0.02% of allfemales develop into queens over a single season (Winston1987; van Veen & Sommeijer 2000).Melipona stingless bees are a unique exception to thispattern (Ratnieks 2001; Wenseleers et al. 2003). In Meli-pona, the adult workers have little power to control thecaste fate of developing females because queens and work-ers are the same size, and are reared in identical sealedcells (Engels & Imperatriz-Fonseca 1990; figure 1). Thisgives individual female larvae the power to determine theirown fate (Bourke & Ratnieks 1999; Ratnieks 2001;Wenseleers et al. 2003; figure 1). Theory shows that inthe pursuit of their individual interests, self-determinationshould result in a TOC in which many more immaturefemales develop into queens than are needed for swarming(Bourke & Ratnieks 1999; Ratnieks 2001; Wenseleers etal. 2003). This general prediction is supported becauseMelipona colonies greatly overproduce queens (Wilson1971; Engels & Imperatriz-Fonseca 1990) (5–16% of allfemales develop into queens; figure 2). This is costly tothe colony as a whole since the excess queens serve nouseful purpose and are swiftly executed by the workersafter they emerge from their cells (Koedam et al. 1995;figure 1). However, inclusive fitness theory also makesmore detailed predictions; in particular, that fewer femalesshould selfishly develop into queens when the cost ofqueen overproduction falls on closer kin (Wenseleers et al.2003). One major factor that affects kinship is the extentof worker reproduction. Workers can lay male eggs. Whenmore of the colony’s males are workers’ sons, the cost ofexcess queen production is borne by more highly relatedindividuals, namely workers’ sons (nephews, r = 0.375)rather than queen’s sons (brothers, r = 0.25). Theory pre-dicts that queen overproduction should be reduced whenmore males are workers’ sons (Ratnieks 2001; Wenseleerset al. 2003). We present the first test, to our knowledge,of this prediction using data on queen production inMelipona species with different degrees of worker repro-duction (figure 2; see electronic Appendix A).2. METHODS(a) Male parentage and caste ratiosTo test the effect of kinship on queen production we collated allavailable data on male parentage and female caste ratio in Melipona.A total of 32 studies and four reviews across 13 species were found.However, we only used studies where male parentage and caste ratiowere known for the same population or geographical region, and weremeasured in either their natural environment or laboratory conditionswhere conditions approached natural ones as closely as possible. Thisproduced 12 studies on four species: Melipona beecheii (three studies,all from Yucatan, Mexico), M. favosa (Tobago, West Indies), M.quadrifasciata (various sites, Brazil) and M. subnitida (Rio Grande doNorte, Brazil) (see tables 1, 2 in electronic Appendix A). Male pro-duction by workers and female caste ratios in these four species areTragedy of the commons in bees T. Wenseleers and F. L. W. Ratnieks S311(a)(b)(c)(d )(e)Q QQQQFigure 1. In Melipona bees queens are the same size asworkers and develop individually in a sealed cell (bold) on aprovision mass (a). This gives female larvae sufficientresources to develop into either caste. In other highlyeusocial bees, Trigonini stingless bees (b) and honey bees(c), the larger queens develop in special cells and theirrearing is under the control of the adult workers who buildand provision the cells. In Melipona, individual control ofcaste development results in a TOC in which many morequeens are reared than are needed ((d) Q, queen pupae incells from which cappings have been removed). Excessqueens are killed by workers (left) soon after emergence (e).summarized in figure 2. Detailed statistics and a complete list of theoriginal studies are available in electronic Appendix A.3. RESULTSAs predicted, in species where many males are workers’sons (M. favosa, Sommeijer et al. 1999; M. quadrifasciata,da Silva 1977; Tóth et al. 2002; M. subnitida, Contel &Kerr 1976; Koedam et al. 1999), fewer females selfishlybecome queens (5.1–8.6%; Kerr 1950; Koedam et al.1999; Sommeijer et al. 2003) than in M. beecheii (15.8%;Darchen & Delage-Darchen 1975; Moo-Valle et al. 2001),where all males are queens’ sons (Paxton et al. 2001) (seetables 1 and 2 in electronic Appendix A). In addition,queen production is lower in M. favosa (5.1%), a speciesin which nearly all males are workers’ sons (Sommeijer etal. 1999), than inM. subnitida (7.1%; Koedam et al. 1999)and M. quadrifasciata (8.6%; Kerr 1950), where 36–51%of the males are workers’ sons (see tables 1 and 2 in elec-tronic Appendix A). The negative relationship betweenqueen overproduction and worker reproduction is signifi-cant ( = 1, Z = 2.04, p = 0.04) and supports the role ofkinship in influencing a tragedy of the commons. Theobserved caste ratios, 5–16%, are slightly lower than thosepredicted by theoretical models (14–20%; Wenseleers etal. 2003). However, these models assume that excessqueen production causes a linear reduction in total colonyproductivity (male and swarm production; Wenseleers etal. 2003). If the cost function were concave, a closermatch between theoretical and empirical figures occursProc. R. Soc. Lond. B (Suppl.)1008060402001612840percentage of maleworkers’ sonspercentage of queensproduced13/108/GEN13/12/10 63814/247/GEN + OBS14/1 338/GEN + OBS4/604/OBS4/2/23839/11/280678/10/13 514sn.s.ssn.s.sM. beecheiiYucatan, MexicoM. subnitidaRio Grande do Norte, BrazilM. quadrifasciatavarious sites, BrazilM. favosaTobago, West Indies(a)(b)Figure 2. The effect of the colony kin structure on queenproduction in Melipona. Theory predicts that fewer femalesshould selfishly develop as queens when many males areworkers’ sons because the cost of excess queen production isthen borne by closer relatives, nephews (r = 0.375) ratherthan brothers (r = 0.25). This prediction is supported bylevels of queen production in Melipona species with variabledegrees of worker reproduction. In Melipona favosa, where(a) nearly all males are workers’ sons, and (b) fewer femalesselfishly become queens (5.1%) than in M. beecheii (15.8%),where all males are queen’s sons. In M. subnitida and M.quadrifasciata, where (a) the queen and the workers sharemale parentage, and (b) queen production is intermediate(7.1 and 8.6%). The negative relationship between queenoverproduction and worker reproduction is significant( = 1, Z = 2.04, p = 0.04). For each data point the mean,95% binomial confidence limit and sample size are shown(number of colonies/months/individuals for queen productiondata and number of colonies/males for male parentage data).For the male parentage data, it is also shown whether thedata come from genetic (GEN) or observational studies(OBS), or both combined (GEN  OBS). Significant( p  0.05) and non-significant ( p  0.05) differencesbetween data points, as indicated from a non-overlap of theconfidence limits, are indicated with ‘s’ and ‘n.s.’. A detailedlist of the source studies on which the comparison is basedis given in electronic Appendix A.(Wenseleers et al. 2003). Importantly, however, a negativerelationship between queen production and worker repro-duction is predicted by the theory irrespective of the exactshape of the cost function. Hence, relative predictions arerobust and independent of detailed assumptions.4. DISCUSSIONWhat general lessons can be learned from the way thatbees resolve tragedies of the commons? TheMelipona caseshows that in a situation where a common resource is freeto be used by all, selfish exploitation is inevitable (Hardin1968, 1998). In this respect, Hardin’s conclusion thatS312 T. Wenseleers and F. L. W. Ratnieks Tragedy of the commons in bees‘freedom in a commons brings ruin to all’ remains (Hardin1968, 1998). Not considered by Hardin (1968, 1998),however, were the effects of kinship. Our results providethe first tentative evidence, to our knowledge, that kinshipcan also partly reduce a TOC. This may be relevant tohuman society, such as in cases where common resourcesare shared by an extended family. However, coercion ismore effective than kinship in resolving a TOC. Considerthe honeybee A. mellifera. Because of multiple mating byqueens, relatedness among offspring females is low (ca.0.30), and the optimum proportion of female larvae thatshould develop into queens, given the ability to do so, isvery high (56%; Wenseleers et al. 2003). However, excessqueen production in honeybees is effectively preventedbecause the adult workers can enforce the caste fate oflarvae by rearing them in distinct cells and on differentfoods (Winston 1987; Beekman et al. 2003; figure 1). Thisshows that nutritional caste determination, found in mostsocial Hymenoptera with morphologically distinct queenand worker castes (Wilson 1971), is actually a form ofsocial suppression that forces individuals to work for thebenefit of society, even when this is against the individuals’own selfish interests. In other words, social insect workersmay usually be oppressed rather than genuinely altruistic(cf. Michener & Brothers 1974; Alonso & Schuck-Paim2002). In human society, social suppression is also wide-spread, but fortunately never reaches the point found inbees where individuals are fated, by their morphology,to work.Alonso, W. J. & Schuck-Paim, C. 2002 Sex-ratio conflicts, kin selec-tion, and the evolution of altruism. Proc. Natl Acad. Sci. USA 99,6843–6847.Beekman, M., Komdeur, J. & Ratnieks, F. L. W. 2003 Reproductiveconflicts in social animals: who has power? Trends Ecol. Evol. 18,277–282.Bourke, A. F. G. & Ratnieks, F. L. W. 1999 Kin conflict over castedetermination in social Hymenoptera. Behav. Ecol. Sociobiol. 46,287–297.Contel, E. P. B. & Kerr, W. E. 1976 Origin of males in Meliponasubnitida estimated from data of an isozymic polymorphic system.Genetica 46, 271–279.Darchen, R. & Delage-Darchen, B. 1975 Contribution à l’étuded’une abeille du Mexique Melipona beecheii B. (Hymenoptère:Apide). Apidologie 6, 295–339.da Silva, D. L. N. 1977 Estudos bionomicos em colônias mistas deMeliponinae. Bol. Zool. São Paulo 2, 7–106.Engels, W. & Imperatriz-Fonseca, V. L. 1990 Caste development,reproductive strategies, and control of fertility in honey bees andstingless bees. In Social insects. An evolutionary approach to castesand reproduction (ed. W. Engels), pp. 167–230. Berlin: Springer.Frank, S. A. 1995 Mutual policing and repression of competition inthe evolution of cooperative groups. Nature 377, 520–522.Proc. R. Soc. Lond. B (Suppl.)Frank, S. A. 1998 The foundations of social evolution. Monographs inbehavior and ecology. Princeton University Press.Hamilton, W. D. 1964 The genetical evolution of social behaviour.Parts I & II. J. Theor. Biol. 7, 1–52.Hardin, G. 1968 The tragedy of the commons. Science 162, 1243–1244.Hardin, G. 1998 Extensions of ‘the tragedy of the commons’. Science280, 682–683.Kerr, W. E. 1950 Genetic determination of castes in the genusMelipona. Genetics 35, 143–152.Koedam, D., Aguilar Monge, I. & Sommeijer, M. J. 1995 Socialinteractions of gynes and their longevity in queenright colonies ofMelipona favosa (Apidae: Meliponinae).Neth. J. Zool. 45, 480–494.Koedam, D., Contrera, F. A. L. & Imperatriz-Fonseca, V. L. 1999Clustered male production by workers in the stingless beeMeliponasubnitida Ducke (Apidae, Meliponinae). Insectes Soc. 46, 387–391.Michener, C. D. & Brothers, D. J. 1974 Were workers of eusocialHymenoptera initially altruistic or oppressed? Proc. Natl Acad. Sci.USA 71, 671–674.Mock, D. W. & Parker, G. 1998 The evolution of sibling rivalry. OxfordUniversity Press.Moo-Valle, H., Quezada-Euan, J. J. G. & Wenseleers, T. 2001 Theeffect of food reserves on the production of sexual offspring in thestingless bee Melipona beecheii (Apidae, Meliponini). Insectes Soc.48, 398–403.Ostrom, E. 1999 Governing the commons. Cambridge UniversityPress.Paxton, R. J., Ruhnke, H., Shah, M., Bego, L. R., Quezada-Euan,J. J. G. & Ratnieks, F. L. W. 2001 Social evolution in stinglessbees: are the workers or is the queen in control of male production?In II Seminario Mexicano sobre abejas sin aguijón (ed. J. J. G.Quezada-Euan), pp. 104–107. Yucatán, México: UniversidadAutónoma de Yucatán, Mérida.Ratnieks, F. L. W. 2001 Heirs and spares: caste conflict and excessqueen production in Melipona bees. Behav. Ecol. Sociobiol. 50,467–473.Sommeijer, M. J., Chinh, T. X. & Meeuwsen, F. J. A. J. 1999 Behav-ioural data on the production of males by workers in the stinglessbeeMelipona favosa (Apidae, Meliponinae). Insectes Soc. 46, 92–93.Sommeijer, M. J., de Bruijn, L. L. M., Meeuwsen, F. J. A. J. & Mar-tens, E. P. 2003 Natural patterns of caste and sex allocation in thestingless bees Melipona favosa and M. trinitatis related to workerbehaviour. Insectes Soc. 50, 38–44.Tóth, E., Strassmann, J. E., Nogueira-Neto, P., Imperatriz-Fonseca,V. L. & Queller, D. C. 2002 Male production in stingless bees:variable outcomes of queen–worker conflict. Mol. Ecol. 11,2661–2667.van Veen, J. W. & Sommeijer, M. J. 2000 Colony reproduction inTetragonisca angustula (Apidae, Meliponini). Insectes Soc. 47, 70–75.Wenseleers, T., Ratnieks, F. L. W. & Billen, J. 2003 Caste fate con-flict in swarm-founding social Hymenoptera: an inclusive fitnessanalysis. J. Evol. Biol. 16, 647–658.Wilson, E. O. 1971 The insect societies. Cambridge, MA: HarvardUniversity Press.Winston, M. L. 1987 The biology of the honey bee. Cambridge, MA:Harvard University Press.Visit www.journals.royalsoc.ac.uk and navigate to this article throughBiology Letters to see the accompanying electronic appendix.

T. Wenseleers

F. L. W. Ratnieks

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Tragedy of the commons in
                    Melipona

In human society selfish use of common resources can lead to disaster, a situation known as the 'tragedy of the commons' (TOC). Although a TOC is usually prevented by coercion, theory predicts that close kinship ties can also favour reduced exploitation. We test this prediction using data on a TOC occurring in Melipona bee societies

T Wenseleers (11637232)

Francis Ratnieks (4461004)

Sussex Research Online

http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1810046

Tragedy of the commons in Melipona bees

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