Abstract
Social parasites exploit the brood care behavior of other species and can exert strong selection pressures on their hosts. As a consequence, hosts have developed defenses to circumvent or to lower the costs of parasitism. Recently, a novel, indirect defense trait, termed slave rebellion, has been described for hosts of a slave-making ant: Enslaved Temnothorax longispinosus workers reduce local parasite pressure by regularly killing pupae of their obligatory slavemaking parasite Protomognathus americanus. Subsequently, growth of social parasite nests is reduced, which leads to fewer raids and likely increases fitness of neighboring related host colonies. In this study, we investigate the presence and expression the slave rebellion trait in four communities. We report its presence in all parasitized communities, document strong variation in its expression between different geographic sites and discuss potential explanations for this observed variation.
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References
Achenbach A, Foitzik S (2009) First evidence for slave rebellion: enslaved ant workers systematically kill the brood of their social parasite Protomognathus Americanus. Evolution 63(4):1068–1075
Achenbach A, Witte V et al (2010) Brood exchange experiments and chemical analyses shed light on slave rebellion in ants. Behav Ecol 21(5):948–956
Alloway TM (1990) Slave-species ant colonies recognize slavemakers as enemies. Anim Behav 39:1218–1220
Beibl J, Stuart RJ et al (2005) Six origins of slavery in Formicoxenine ants. Insectes Soc 52(3):291–297
Berdoy M, Webster JP et al (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc R Soc Lond B Biol Sci 267(1452):1591–1594
Brandt M, Foitzik S (2004) Community context and specialization influence coevolution between a slavemaking ant and its hosts. Ecology 85(11):2997–3009
Brandt M, Heinze J et al (2005) A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J Evol Biol 18(3):576–586
Brandt M, Heinze J et al (2006) Convergent evolution of the Dufour’s gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus. Insectes Soc 53(3):291–299
Brandt M, Fischer-Blass B et al (2007) Population structure and the co-evolution between social parasites and their hosts. Mol Ecol 16(10):2063–2078
Britton NF, Planque R, Franks NR (2007) Evolution of defence portfolios in exploiter-victim systems. Bull Math Biol 69(3):957–988. doi:10.1007/s11538-006-9178-5
Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235
Clay K (1991) Parasitic castration of plants by fungi. Trends Ecol Evol 6(5):162–166
Davies NB (1999) Cuckoos and cowbirds versus hosts: co-evolutionary lag and equilibrium. Ostrich 70(1):71–79
Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B Biol Sci 205(1161):489–511
Fischer-Blass B, Heinze J et al (2006) Microsatellite analysis reveals strong but differential impact of a social parasite on its two host species. Mol Ecol 15(3):863–872
Foitzik S, Herbers JM (2001a) Colony structure of a slavemaking ant. I. Intracolony relatedness, worker reproduction, and polydomy. Evolution 55(2):307–315
Foitzik S, Herbers JM (2001b) Colony structure of a slavemaking ant. II. Frequency of slave raids and impact on the host population. Evolution 55(2):316–323
Foitzik S, DeHeer CJ et al (2001) Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts. Proc R Soc Lond B Biol Sci 268(1472):1139–1146
Foitzik S, Achenbach A et al (2009) Locally adapted social parasite affects density, social structure, and life history of its ant hosts. Ecology 90(5):1195–1206
Gladstone DE (1981) Why there are no ant slave rebellions. Am Nat 117(5):779–781
Hare JF, Alloway TM (2001) Prudent Protomognathus and despotic Leptothorax duloticus: differential costs of ant slavery. Proc Nat Acad Sci USA 98(21):12093–12096
Hefetz A (2007) The evolution of hydrocarbon pheromone parsimony in ants (Hymenoptera: Formicidae)—interplay of colony odor uniformity and odor idiosyncrasy. A review. Myrmecol News 10:59–68
Herbers JM, Foitzik S (2002) The ecology of slavemaking ants and their hosts in north temperate forests. Ecology 83(1):148–163
Kruger O (2007) Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Philos Transact R Soc B Biol Sci 362(1486):1873–1886
Lafferty KD, Kuris AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol 25(12):564–572
Langmore NE, Hunt S et al (2003) Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422(6928):157–160
Lorenzana JC, Sealy SG (2001) Fitness costs and benefits of cowbird egg ejection by gray catbirds. Behav Ecol 12(3): 325–329. doi:10.1093/beheco/12.3.325
Lorenzi MC, Thompson JN (2011) The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution. Evolution 65(12):3527–3542
Moksnes A, Roskaft E et al (1991) Behavioral-responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–89
Pamminger T, Scharf I, Pennings PS, Foitzik S (2011) Increased host aggression as a induced defence against slave-making ants. Behav Ecol 22(2):255–260
Pennings PS, Achenbach A et al (2011) Similar evolutionary potentials in an obligate ant parasite and its two host species. J Evol Biol 24(4):871–886
Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version 3.1-101
Price PW (1980) Evolutionary biology of parasites. Princeton University Press, Princeton
Roskaft E, Moksnes A et al (2002) Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139:613–628
Rothstein SI (1990) A model system for coevolution—avian brood parasitism. Annu Rev Ecol Syst 21:481–508
Sato T (1986) A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323(6083):58–59
Scharf I, Pamminger T, Foitzik S (2011) Differential response of ant colonies to intruders: attack strategies correlate with potential threat. Ethology 117(8):731–739
Soler M, Moller AP (1990) Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343(6260):748–750
Stokke BG, Hafstad I et al (2008) Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol 19:612–620
Thomas F, Adamo S et al (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68(3):185–199
Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago, IL
Vikan JR, Stokke BG et al (2010) Evolution of defences against cuckoo (Cuculus canorus) parasitism in bramblings (Fringilla montifringilla): a comparison of four populations in Fennoscandia. Evol Ecol 24:1141–1157
Yu DW, Pierce NE (1998) A castration parasite of an ant-plant mutualism. Proc R Soc Lond B Biol Sci 265(1394):375–382
Acknowledgments
We like to thank the two anonymous reviewers and the associate editor for their time and constructive criticism which substantially improved the quality of the manuscript. Funding was by the Deutsche Forschungsgemeinschaft Research Unit 1078 grant Fo 298/9-1 and E.N. Huyck Preserve.
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Pamminger, T., Leingärtner, A., Achenbach, A. et al. Geographic distribution of the anti-parasite trait “slave rebellion”. Evol Ecol 27, 39–49 (2013). https://doi.org/10.1007/s10682-012-9584-0
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DOI: https://doi.org/10.1007/s10682-012-9584-0