The host-parasite genera Proformica-Rossomyrmex present four pairs of species with a very wide range of distribution from China to Southeastern Spain, from huge extended plains to the top of high mountains. Here we review (1) the published data on these pairs in comparison to other slave-makers; (2) the different dispersal ability in hosts and parasites inferred from genetics (chance of migration conditions the evolutionary potential of the species); (3) the evolutionary potential of host and parasite determining the coevolutionary process in each host-parasite system that we treat to define using cuticular chemical data. We find a lower evolutionary potential in parasites than in hosts in fragmented populations, where selective pressures give advantage to a limited female parasite migration due to uncertainty of locating a host nest. A similar evolutionary potential is detected for hosts and parasites when the finding of host nests is likely (i.e., in continuous and extended populations). Moreover, some level of local adaptation at CHC profiles between host and parasite exists independently of the kind of geographic distribution and the ability of dispersal of the different populations. Similarity at CHC profiles appears to be a trait imposed by natural selection for the interaction between hosts and slave-makers. 1. Introduction Slave-making ants are a type of permanent social parasites (thus depending on enslaved hosts ants throughout their whole live) whose newly mated queens need to usurp a host nest in order to initiate a new parasite colony. Then the host brood will turn into slaves working for the parasite species while parasite workers only concentrate on replenishing the labour force from neighboring host nests, a process called slave raiding (see reviews [1–4]). The slave-maker style of life imposes selection pressures to both parts, as frequent slave raids strongly affect host populations and on the other hand, invading a host nest by parasite queens is determinant for their survival (see [2, 5, 6]). In this sense the study of host-parasite systems allows the study of coevolutionary strategies. Within the subfamily Formicinae only two genera fit the previous definition of slave-makers: Polyergus and Rossomyrmex [5–7]. The species of the Formica sanguinea group are facultative slave-makers [8, 9]. Thus, in relation with the obligate slave-maker genera most of the published studies are focused on Polyergus biology (e.g., [10–15]) whereas the genus Rossomyrmex has received little attention, probably due to its geographic distribution and
References
[1]
A. Buschinger, “Evolution of social parasitism in ants,” Trends in Ecology and Evolution, vol. 1, no. 6, pp. 155–160, 1986.
[2]
H. Topoff, “Slave-making queens,” Scientific American, vol. 281, no. 5, pp. 84–90, 1999.
[3]
P. D'Ettorre and J. Heinze, “Sociobiology of slave-making ants,” Acta Ethologica, vol. 3, no. 2, pp. 67–82, 2001.
[4]
A. Buschinger, “Social parasitism among ants: a review (Hymenoptera: Formicidae),” Myrmecological News, vol. 12, pp. 219–235, 2009.
[5]
E. O. Wilson, The Insect Societies, Belknap Press, Cambridge, Mass, USA, 1971.
[6]
A. Mori and F. Le Moli, “Behavioural plasticity and domestic degeneration in facultative and obligatory slave-making ant species (Hymenoptera, Formicidae),” Monitore Zoologico Italiano, vol. 22, pp. 271–285.
[7]
F. Ruano and A. Tinaut, “Raid process, activity pattern and influence of abiotic conditions in the slave-making ant Rossomyrmex minuchae (Hymenoptera, Formicidae) a slave-maker species,” Insectes Sociaux, vol. 46, no. 4, pp. 341–347, 1999.
[8]
B. H. H?lldobler and E. O. Wilson, The Ants, Springer, Berlin, Germany, 1990.
[9]
A. Mori, D. A. Grasso, R. Visicchio, and F. Le Moli, “Comparison of reproductive strategies and raiding behaviour in facultative and obligatory slave-making ants: the case of Formica sanguinea and Polyergus rufescens,” Insectes Sociaux, vol. 48, no. 4, pp. 302–314, 2001.
[10]
M. Talbot, “Slave-raids of the ant Polyergus lucidus Mayr,” Psyche, vol. 74, pp. 199–231, 1967.
[11]
H. Topoff and L. Greenberg, “Mating behavior of the socially-parasitic ant, Polyergus breviceps: the role of the mandibular glands,” Psyche, vol. 95, pp. 81–88, 1988.
[12]
F. Le Moli, D. A. Grasso, A. Mori, and A. Ugolini, “Eco-ethological factors affecting the scouting and raiding behaviour of the slave-making ant Polyergus rufescens Latr. (Hymenoptera, Formicidae),” Ethology, vol. 96, no. 4, pp. 289–302, 1994.
[13]
A. Mori, D. A. Grasso, P. D'Etorre, and F. Le Moli, “Specifity in host choice by the slave-making ant Polyergus rufescens Latr. (Hymenoptera, Formicidae),” Ethology, Ecology & Evolution, vol. 3, pp. 89–93, 1994.
[14]
S. Boi, V. Capasso, and D. Morale, “Modeling the aggregative behavior of ants of the species Polyergus rufescens,” Nonlinear Analysis: Real World Applications, vol. 1, no. 1, pp. 163–176, 2000.
[15]
C. A. Johnson, H. Topoff, R. K. Vander Meer, and B. Lavine, “Do these eggs smell funny to you? An experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae),” Behavioral Ecology and Sociobiology, vol. 57, no. 3, pp. 245–255, 2005.
[16]
F. Ruano and A. Tinaut, “The assault process of the slave-making ant Rossomyrmex minuchae (Hymenoptera, Formicidae),” Sociobiology, vol. 43, no. 2, pp. 201–209, 2004.
[17]
F. Ruano and A. Tinaut, “Mating behaviour in a slave-making ant, Rossomyrmex minuchae (Hymenoptera, Formicidae),” Naturwissenschaften, vol. 92, no. 7, pp. 328–331, 2005.
[18]
K. V. Arnoldi, “Biologische beobachtungen an der neuen pal?arktischen sklavenhalterameise Rossomyrmex froformicarum K. Arn., Nebst einigen bemerkungen über die bef?rderungsweise der ameisen,” Zeitschrift für Morphologie und ?kologie der Tiere, vol. 24, no. 2, pp. 319–326, 1932.
[19]
P. I. Marikovsky, “The biology of the ant Rossomyrmex proformicarum K. W. Arnoldi (1928),” Insectes Sociaux, vol. 21, no. 3, pp. 301–308, 1974.
[20]
O. Sanllorente, R. L. Hammond, F. Ruano, L. Keller, and A. Tinaut, “Extreme population differentiation in a vulnerable slavemaking ant with a fragmented distribution,” Conservation Genetics, vol. 11, no. 5, pp. 1701–1710, 2010.
[21]
A. Mori, P. D. 'Ettorre, and F. Le Moli, “Mating and post-mating behaviour of the European amazon ant, Polyergus rufescens (Hymenoptera, Formicidae),” Bolletino Zoologia, vol. 61, pp. 203–206, 1994.
[22]
U. Winter and A. Buschinger, “Genetically mediated queen polymorphism and caste determination in the slave-making ant Harpagoxenus sublaevis (Hymenoptera: Formicidae),” Entomologia Generalis, vol. 11, pp. 125–137, 1986.
[23]
F. Ruano, A. Hefetz, A. Lenoir, W. Francke, and A. Tinaut, “Dufour's gland secretion as a repellent used during usurpation by the slave-maker ant Rossomyrmex minuchae,” Journal of Insect Physiology, vol. 51, no. 10, pp. 1158–1164, 2005.
[24]
C. Zamora-Mu?oz, F. Ruano, C. Errard, A. Lenoir, A. Hefetz, and A. Tinaut, “Coevolution in the slave-parasite system Proformica longiseta-Rossomyrmex minuchae (Hymenoptera: Formicidae),” Sociobiology, vol. 42, no. 2, pp. 299–317, 2003.
[25]
L. van Oudenhove, R. Boulay, A. Lenoir, C. Bernstein, and X. Cerdá, “Substrate temperature constrains recruitment and trail following behavior in ants,” Journal of Chemical Ecology, vol. 38, pp. 802–809, 2012.
[26]
A. Tinaut and F. Ruano, “Braquipterismo y apterismo en Formícidos. Morfología y biometría en las hembras de especies ibéricas de vida libre (Hymenoptera, Formicidae),” Graellsia, vol. 48, pp. 121–131, 1992.
[27]
A. Tinaut, “Rossomyrmex minuchae nov. sp. (Hym. Formicidae) encontrada en Sierra Nevada, Espa?a,” Boletín de la Asociación espa?ola de Entomología, vol. 4, pp. 195–203, 1981.
[28]
A. Tinaut, F. Ruano, and I. Fernández-Escudero, “Descripción del macho del género Rossomyrmex Arnoldi, 1928 (Hymenoptera, Formicidae),” Nouvelle Revue d'Entomologie, vol. 4, pp. 347–351, 1994.
[29]
J. Clobert, E. Danchin, A. A. Dhondt, and J. D. Nichols, Dispersal, Oxford University Press, New York, NY, USA, 2001.
[30]
M. Brandt, J. Heinze, T. Schmitt, and S. Foitzik, “A chemical level in the coevolutionary arms race between an ant social parasite and its hosts,” Journal of Evolutionary Biology, vol. 18, no. 3, pp. 576–586, 2005.
[31]
S. Gandon, Y. Capowiez, Y. Dubois, Y. Michalakis, and I. Olivieri, “Local adaptation and gene-for-gene coevolution in a metapopulation model,” Proceedings of the Royal Society B, vol. 263, no. 1373, pp. 1003–1009, 1996.
[32]
S. Gandon, “Local adaptation and the geometry of host-parasite coevolution,” Ecology Letters, vol. 5, no. 2, pp. 246–256, 2002.
[33]
R. Frankham, J. D. Ballou, and D. A. Briscoe, Introduction to Conservation Genetics, Cambridge University Press, Cambridge, UK, 2002.
[34]
O. Sanllorente, P. Lorite, S. Devers, F. Ruano, A. Lenoir, and A. Tinaut, “The spatial distribution does not affect host-parasite coevolution in Rossomyrmex ants,” Insectes Sociaux, vol. 59, pp. 361–368, 2012.
[35]
S. Gandon and Y. Michalakis, “Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time,” Journal of Evolutionary Biology, vol. 15, no. 3, pp. 451–462, 2002.
[36]
M. Brandt, B. Fischer-Blass, J. Heinze, and S. Foitzik, “Population structure and the co-evolution between social parasites and their hosts,” Molecular Ecology, vol. 16, no. 10, pp. 2063–2078, 2007.
[37]
P. S. Pennings, A. Achenbach, and S. Foitzik, “Similar evolutionary potentials in an obligate ant parasite and its two host species,” Journal of Evolutionary Biology, vol. 24, no. 4, pp. 871–886, 2011.
[38]
S. Foitzik, S. Bauer, S. Laurent, and P. S. Pennings, “Genetic diversity, population structure and sex-biased dispersal in three co-evolving species,” Journal of Evolutionary Biology, vol. 22, no. 12, pp. 2470–2480, 2009.
[39]
F. Ruano, S. Devers, O. Sanllorente, C. Errard, A. Tinaut, and A. Lenoir, “A geographical mosaic of coevolution in a slave-making host-parasite system,” Journal of Evolutionary Biology, vol. 24, no. 5, pp. 1071–1079, 2011.
[40]
P. D’Ettorre and A. Lenoir, “Nestmate recognition in ants,” in Ant Ecology, L. Lach, C. Parr, and K. Abbott, Eds., pp. 194–209, Oxford University Press, Oxford, UK, 2010.
[41]
K. A. Copren, L. J. Nelson, E. L. Vargo, and M. I. Haverty, “Phylogenetic analyses of mtDNA sequences corroborate taxonomic designations based on cuticular hydrocarbons in subterranean termites,” Molecular Phylogenetics and Evolution, vol. 35, no. 3, pp. 689–700, 2005.
[42]
S. J. Martin, H. Helanter?, and F. P. Drijfhout, “Evolution of species-specific cuticular hydrocarbon patterns in Formica ants,” Biological Journal of the Linnean Society, vol. 95, no. 1, pp. 131–140, 2008.
[43]
A. Lenoir, P. D'Ettorre, and C. Errard, “Chemical ecology and social parasitism in ants,” Annual Review of Entomology, vol. 46, pp. 573–599, 2001.
[44]
E. Nowbahari, A. Lenoir, J. L. Clément, C. Lange, A. G. Bagneres, and C. Joulie, “Individual, geographical and experimental variation of cuticular hydrocarbons of the ant Cataglyphis cursor (Hymenoptera: Formicidae): their use in nest and subspecies recognition,” Biochemical Systematics and Ecology, vol. 18, no. 1, pp. 63–74, 1990.
[45]
D. R. Nash, T. D. Als, R. Maile, G. R. Jones, and J. J. Boomsma, “A mosaic of chemical coevolution in a large blue butterfly,” Science, vol. 319, no. 5859, pp. 88–90, 2008.
[46]
L. V. Ugelvig, F. P. Drijfhout, D. J. C. Kronauer, J. J. Boomsma, J. S. Pedersen, and S. Cremer, “The introduction history of invasive garden ants in Europe: integrating genetic, chemical and behavioural approaches,” BMC Biology, vol. 6, article 11, 2008.
[47]
I. Fernández-Escudero and A. Tinaut, “Factors determining nest distribution in the high-mountain ant Proformica longiseta (Hymenoptera Formicidae),” Ethology Ecology and Evolution, vol. 11, no. 4, pp. 325–338, 1999.
[48]
S. Dronnet, C. Lohou, J.-P. Christides, and A.-G. Bagnères, “Cuticular hydrocarbon composition reflects genetic relationship among colonies of the introduced termite Reticulitermes santonensis feytaud,” Journal of Chemical Ecology, vol. 32, no. 5, pp. 1027–1042, 2006.
[49]
A. Tinaut, F. Ruano, O. Sanllorente, A. Fernández-Zambrano, C. Karaman, and Y. Kaz, “Nest composition and worker relatedness in three slave-making ants of the genus Rossomyrmex Arnoldi and their Proformica Ruzsky hosts (Hymenoptera, Formicidae),” Insect Science, vol. 17, no. 4, pp. 361–368, 2010.
[50]
B. Fischer and S. Foitzik, “Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system,” Journal of Evolutionary Biology, vol. 17, no. 5, pp. 1026–1034, 2004.