zbMATH — the first resource for mathematics

Evolution of worker policing. (English) Zbl 1347.92113
Summary: Workers in insect societies are sometimes observed to kill male eggs of other workers, a phenomenon known as worker policing. We perform a mathematical analysis of the evolutionary dynamics of policing. We investigate the selective forces behind policing for both dominant and recessive mutations for different numbers of matings of the queen. The traditional, relatedness-based argument suggests that policing evolves if the queen mates with more than two males, but does not evolve if the queen mates with a single male. We derive precise conditions for the invasion and stability of policing alleles. We find that the relatedness-based argument is not robust with respect to small changes in colony efficiency caused by policing. We also calculate evolutionarily singular strategies and determine when they are evolutionarily stable. We use a population genetics approach that applies to dominant or recessive mutations of any effect size.
92D50 Animal behavior
92D15 Problems related to evolution
Full Text: DOI
[1] Abbot, P., Inclusive fitness theory and eusociality, Nature, 471, E1-E9, (2011)
[2] Akcay, E.; Van Cleve, J., There is no fitness but fitness, and the lineage is its bearer, Philos. Trans. R. Soc. B, 371, 20150085, (2016)
[3] Allen, B.; Nowak, M. A.; Wilson, E. O., Limitations of inclusive fitness, Proc. Natl. Acad. Sci. U.S.A., 110, 20135-20139, (2013) · Zbl 1355.91057
[4] Allen, B.; Nowak, M. A., Games on graphs, EMS Surv. Math. Sci., 1, 1, 115-151, (2014) · Zbl 1303.91040
[5] Antal, T.; Scheuring, I., Fixation of strategies for an evolutionary game in finite populations, Bull. Math. Biol., 68, 1923-1944, (2006) · Zbl 1296.92238
[6] Antal, T.; Ohtsuki, H.; Wakeley, J.; Taylor, P. D.; Nowak, M. A., Evolution of cooperation by phenotypic similarity, Proc. Natl. Acad. Sci. U.S.A., 106, 21, 8597-8600, (2009) · Zbl 1355.92145
[7] Beekman, M.; Oldroyd, B. P., Honeybee workers use cues other than egg viability for policing, Biol. Lett., 1, 129-132, (2005)
[8] Birch, J.; Okasha, S., Kin selection and its critics, BioScience, 65, 22-32, (2014)
[9] Bonckaert, W.; Vuerinckx, K.; Billen, J.; Hammond, R. L.; Keller, L.; Wenseleers, T., Worker policing in the German wasp vespula germanica, Behav. Ecol., 19, 272-278, (2008)
[10] Bonckaert, W.; van Zweden, J. S.; d׳Ettorre, P.; Billen, J.; Wenseleers, T., Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp, Mol. Ecol., 20, 3455-3468, (2011)
[11] Boomsma, J. J., Kin selection versus sexual selectionwhy the ends do not meet, Curr. Biol., 17, R673-R683, (2007)
[12] Boomsma, J. J., Lifetime monogamy and the evolution of eusociality, Philos. Trans. R. Soc. B, 364, 3191-3207, (2009)
[13] Bourke, A. F.G., The validity and value of inclusive fitness theory, Proc. R. Soc. B, 278, 3313-3320, (2011)
[14] Cavalli-Sforza, L. L.; Feldman, M. W., Darwinian selection and “altruism”, Theor. Popul. Biol., 14, 268-280, (1978) · Zbl 0432.92017
[15] Cole, B. J., The social behavior of leptothorax allardycei (hymenoptera, formicidae)time budgets and the evolution of worker reproduction, Behav. Ecol. Sociobiol., 18, 165-173, (1986)
[16] Cornwallis, C. K.; West, S. A.; Davis, K. E.; Griffin, A. S., Promiscuity and the evolutionary transition to complex societies, Nature, 466, 969-972, (2010)
[17] Dieckmann, U.; Law, R., The dynamical theory of coevolutiona derivation from stochastic ecological processes, J. Math. Biol., 34, 579-612, (1996) · Zbl 0845.92013
[18] Endler, A.; Liebig, J.; Schmitt, T.; Parker, J. E.; Jones, G. R.; Schreier, P.; Holldobler, B., Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect, Proc. Natl. Acad. Sci. U.S.A., 101, 2945-2950, (2004)
[19] Foster, K. R.; Ratnieks, F. L.W., Facultative worker policing in a wasp, Nature, 407, 692-693, (2000)
[20] Foster, K. R.; Ratnieks, F. L.W., Convergent evolution of worker policing by egg eating in the honeybee and common wasp, Proc. R. Soc. Lond. B, 268, 169-174, (2001)
[21] Foster, K. R.; Ratnieks, F. L.W., The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies, Am. Nat., 158, 615-624, (2001)
[22] Foster, K. R.; Ratnieks, F. L.W., Paternity, reproduction and conflict in vespine waspsa model system for testing kin selection predictions, Behav. Ecol. Sociobiol., 50, 1-8, (2001)
[23] Foster, K. R.; Gulliver, J.; Ratnieks, F. L.W., Worker policing in the European hornet vespa crabro, Insectes Soc., 49, 41-44, (2002)
[24] Foster, K. R.; Wenseleers, T.; Ratnieks, F. L.W., Kin selection is the key to altruism, Trends Ecol. Evol., 21, 57-60, (2006)
[25] Frank, S. A., Foundations of social evolution, (1983), Princeton University Press Princeton, NJ
[26] Fu, F.; Kocker, S. D.; Nowak, M. A., The risk-return trade-off between solitary and eusocial reproduction, Ecol. Lett., 18, 1, 74-84, (2014)
[27] Gadagkar, R., The social biology of ropalidia marginata: toward understanding the evolution of eusociality, (2001), Harvard University Press Cambridge, MA
[28] Gadagkar, R., Why do honey bee workers destroy each other׳s eggs?, J. Biosci., 29, 3, 213-217, (2004)
[29] Gardner, A.; West, S. A.; Wild, G., The genetical theory of kin selection, J. Evol. Biol., 24, 1020-1043, (2011)
[30] Geritz, S. A.H.; Kisdi, E.; Meszena, G.; Metz, J. A.J., Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree, Evol. Ecol., 12, 35-57, (1998)
[31] Hamilton, W. D., Altruism and related phenomena, mainly in social insects, Annu. Rev. Ecol. Syst., 31, 193-232, (1972)
[32] Hammond, R. L.; Keller, L., Conflict over male parentage in social insects, PLoS Biol., 2, e248, 1472-1482, (2004)
[33] Hartmann, A.; Wantia, J.; Torres, J. A.; Heinze, J., Worker policing without genetic conflicts in a clonal ant, Proc. Natl. Acad. Sci. U.S.A., 100, 12836-12840, (2003)
[34] Hauert, C.; Doebeli, M., Spatial structure often inhibits the evolution of cooperation in the snowdrift game, Nature, 428, 643-646, (2004)
[35] Helantera, H.; Tofilski, A.; Wenseleers, T.; Ratnieks, F. L.W., Worker policing in the common wasp vespula vulgaris is not aimed at improving colony hygiene, Insectes Soc., 53, 399-402, (2006)
[36] Helantera, H.; Sundstrom, L., Worker reproduction in formica ants, Am. Nat., 170, E14-E25, (2007)
[37] Hofbauer, J.; Sigmund, K., Adaptive dynamics and evolutionary stability, Appl. Math. Lett., 3, 75-79, (1990) · Zbl 0709.92015
[38] Hughes, W. O.H.; Oldroyd, B. P.; Beekman, M.; Ratnieks, F. L.W., Ancestral monogamy shows kin selection is key to the evolution of eusociality, Science, 320, 1213-1216, (2008)
[39] Kapheim, K. M.; Pan, H.; Li, C.; Salzberg, S. L.; Puiu, D., Genomic signatures of evolutionary transitions from solitary to group living, Science, 348, 1139-1143, (2015)
[40] Khila, A.; Abouheif, E., Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies, Proc. Natl. Acad. Sci. U.S.A., 105, 17884-17889, (2008)
[41] Lehmann, L.; Alger, I.; Weibull, J., Does evolution lead to maximizing behavior?, Evolution, 69, 1858-1873, (2015)
[42] Matessi, C.; Karlin, S., On the evolution of altruism by kin selection, Proc. Natl. Acad. Sci. U.S.A., 81, 1754-1758, (1984)
[43] Metz, J. A.J.; Geritz, S. A.H.; Meszena, G.; Jacobs, F. J.A.; van Heerwaarden, J. S., Adaptive dynamics, a geometrical study of the consequences of nearly faithful reproduction, (van Strien, S. J.; Verduyn Lunel, S. M., Stochastic and Spatial Structures of Dynamical Systems, (1996), KNAW Verhandelingen, Afd. Amsterdam), 183-231 · Zbl 0972.92024
[44] Naeger, N. L.; Peso, M.; Even, N.; Barron, A. B.; Robinson, G. E., Altruistic behavior by egg-laying worker honeybees, Curr. Biol., 23, 1574-1578, (2013)
[45] Nonacs, P., Nepotism and brood reliability in the suppression of worker reproduction in the eusocial hymenoptera, Biol. Lett., 2, 577-579, (2006)
[46] Nowak, M. A.; Sigmund, K., The evolution of stochastic strategies in the prisoner׳s dilemma, Acta Appl. Math., 20, 247-265, (1990) · Zbl 0722.90092
[47] Nowak, M. A.; Tarnita, C. E.; Wilson, E. O., The evolution of eusociality, Nature, 466, 1057-1062, (2010)
[48] Okasha, S.; Martens, J., Hamilton׳s rule, inclusive fitness maximization, and the goal of individual behaviour in symmetric two-player games, J. Evol. Biol., 29, 473-482, (2016)
[49] Olejarz, J. W.; Allen, B.; Veller, C.; Nowak, M. A., The evolution of non-reproductive workers in insect colonies with haplodiploid genetics, eLife, 4, e08918, (2015)
[50] Peters, J. M.; Queller, D. C.; Imperatriz-Fonseca, V. L.; Roubik, D. W.; Strassmann, J. E., Mate number, kin selection and social conflicts in stingless bees and honeybees, Proc. R. Soc. Lond. B, 266, 379-384, (1999)
[51] Pirk, C. W.W.; Neumann, P.; Hepburn, R.; Moritz, R. F.A.; Tautz, J., Egg viability and worker policing in honey bees, Proc. Natl. Acad. Sci. U.S.A., 101, 8649-8651, (1999)
[52] Queller, D. C., A general model for kin selection, Evolution, 46, 376-380, (1992)
[53] Queller, D. C.; Strassmann, J. E., Kin selection and social insects, Bioscience, 48, 165-175, (1998)
[54] Ratnieks, F. L.W., Reproductive harmony via mutual policing by workers in eusocial hymenoptera, Am. Nat., 132, 217-236, (1988)
[55] Ratnieks, F. L.W.; Visscher, P. K., Worker policing in the honeybee, Nature, 342, 796-797, (1989)
[56] Ratnieks, F. L.W.; Foster, K. R.; Wenseleers, T., Conflict resolution in insect societies, Annu. Rev. Entomol., 51, 581-608, (2006)
[57] Seeley, T. D., Honeybee ecology: A study of adaptation in social life, (1985), Princeton University Press Princeton, NJ
[58] Simon, B.; Fletcher, J. A.; Doebeli, M., Towards a general theory of group selection, Evolution, 67, 1561-1572, (2013)
[59] Starr, C.K., 1984. In: Smith, R.L. (Ed.). Sperm Competition, Kinship, and Sociality in the Aculeate Hymenoptera. Academic Press, Orlando, Florida, pp. 427-464.
[60] Szabo, G.; Fath, G., Evolutionary games on graphs, Phys. Rep., 446, 97-216, (2007)
[61] Tarnita, C.E., Taylor, P.D., 2014. Measures of relative fitness of social behaviors in finite structured population models. Am. Nat. 184(4) in press.
[62] Traulsen, A.; Shoresh, N.; Nowak, M. A., Analytical results for individual and group selection of any intensity, Bull. Math. Biol., 70, 1410-1424, (2008) · Zbl 1144.92035
[63] Uyenoyama, M. K.; Feldman, M., Population genetic theory of kin selection. II. the multiplicative model, Am. Nat., 120, 614-627, (1982)
[64] van Veelen, M.; Luo, S.; Simon, B., A simple model of group selection that cannot be analyzed with inclusive fitness, J. Theor. Biol., 360, 279-289, (2014) · Zbl 1343.92372
[65] Velthuis, H. H.W.; de Araujo Alves, D.; Imperatriz-Fonseca, V. L.; Jose, M., Worker bees and the fate of their eggs, Proc. Exp. Appl. Entomol. NEV Amsterdam, 13, 97-102, (2002)
[66] Wenseleers, T.; Helantera, H.; Hart, A.; Ratnieks, F. L.W., Worker reproduction and policing in insect societiesan ESS analysis, J. Evol. Biol., 17, 1035-1047, (2004)
[67] Wenseleers, T.; Hart, A. G.; Ratnieks, F. L.W., When resistance is uselesspolicing and the evolution of reproductive acquiescence in insect societies, Am. Nat., 164, E154-E167, (2004)
[68] Wenseleers, T.; Badcock, N. S.; Erven, K.; Tofilski, A.; Nascimento, F. S.; Hart, A. G.; Burke, T. A.; Archer, M. E.; Ratnieks, F. L.W., A test of worker policing theory in an advanced eusocial wasp, vespula rufa, Evolution, 59, 1306-1314, (2005)
[69] Wenseleers, T.; Ratnieks, F. L.W., Enforced altruism in insect societies, Nature, 444, 50, (2006)
[70] Wenseleers, T.; Ratnieks, F. L.W., Comparative analysis of worker reproduction and policing in eusocial hymenoptera supports relatedness theory, Am. Nat., 168, E163-E179, (2006)
[71] Wenseleers, T.; Helantera, H.; Alves, D. A.; Duenez-Guzman, E.; Pamilo, P., Towards greater realism in inclusive fitness modelsthe case of worker reproduction in insect societies, Biol. Lett., 9, 20130334, (2013)
[72] Wilson, E. O., The insect societies, (1971), Harvard University Press Cambridge, MA
[73] Woyciechowski, M.; Lomnicki, A., Multiple mating of queens and the sterility of workers among eusocial hymenoptera, J. Theor. Biol., 128, 317-327, (1987)
[74] Zanette, L. R.S.; Miller, S. D.L.; Faria, C. M.A.; Almond, E. J.; Huggins, T. J.; Jordan, W. C.; Bourke, A. F.G., Reproductive conflict in bumblebees and the evolution of worker policing, Evolution, 66, 3765-3777, (2012)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.