Among social parasites, workerless inquilines entirely depend on their host for survival and reproduction. They are usually close phylogenetic relatives of their host, which raises important questions about their evolutionary history and mechanisms of speciation at play. Here we present new findings on Ectatomma parasiticum, the only inquiline ant described in the Ectatomminae subfamily. Field data confirmed its rarity and local distribution in a facultative polygynous population of E. tuberculatum in Mexico. Genetic analyses demonstrated that the parasite is a sibling species of its host, from which it may have diverged recently. Polygyny is suggested to have favored the evolution of social parasite by sympatric speciation. Nevertheless, host workers from this population were able to discriminate parasites from their conspecifics. They treated the parasitic queens either as individuals of interest or as intruders, depending on their colonial origin, probably because of the peculiar chemical profile of the parasites and/or their reproductive status. We suggest that E. parasiticum could have conserved from its host sibling species the queen-specific substances that produce attracting and settling effect on workers, which, in return, would increase the probability to be detected. This hypothesis could explain the imperfect social integration of the parasite into host colonies. 1. Introduction Parasitism is found at all levels of biological organization from genes to societies. Social parasites are specialized in exploiting the social living conditions of one or several species [1]. They have evolved manifold in social Hymenoptera, especially in ants where they occur with a huge diversity [1–3]. Parasitic ants can take advantage of the host-colony resources only during the phase of colony founding (temporary social parasitism) or throughout their life cycle, either by raiding host brood and then enslaving workers (slave-making) or by cohabiting in the nest alongside the host queens (inquilinism) [1–3]. In the most derived form, inquilines have developed a set of adaptations such as the loss of the worker caste and a reduced body size (the “inquiline syndrome” [4]). Typically, social parasites and their respective hosts are close phylogenetic relatives. This trend has been formalized as Emery’s rule and generalized in two versions [5, 6]. In the strict version, the parasite is a sibling species of its host; in the loose version, the parasite and the host are nonsiblings but belong to the same or a closely related genus. Some empirical studies support the
References
[1]
A. Buschinger, “Social parasitism among ants: a review (Hymenoptera: Formicidae),” Myrmecological News, vol. 12, pp. 219–235, 2009.
[2]
B. H？lldobler and E. O. Wilson, The Ants, Springer, Berlin, Germany, 1990.
[3]
D. R. Nash and J. J. Boomsma, “Communication between hosts and social parasites,” in Sociobiology of Communication: An Interdisciplinary Perspective, P. d'Ettorre and D. Hughes, Eds., pp. 55–79, Oxford University Press, Oxford, UK, 2008.
[4]
E. O. Wilson, The Insect Societies, Belknap Press of Havard University Press, Cambridge, Mass, USA, 1971.
[5]
G. Le Masne, “Recherches sur les fourmis parasites. Plagiolepis grassei et l'évolution des Plagiolepis parasites,” Comptes rendus de l'Académie des Sciences, vol. 243, pp. 673–675, 1956.
[6]
A. F. G. Bourke and N. R. Franks, “Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants,” Biological Journal of the Linnean Society, vol. 43, no. 3, pp. 157–178, 1991.
[7]
R. Savolainen and K. Veps？l？inen, “Sympatric speciation through intraspecific social parasitism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 12, pp. 7169–7174, 2003.
[8]
S. Sumner, D. K. Aanen, J. Delabie, and J. J. Boomsma, “The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery's rule,” Insectes Sociaux, vol. 51, no. 1, pp. 37–42, 2004.
[9]
J. A. Smith, S. M. Tierney, Y. C. Park, S. Fuller, and M. P. Schwarz, “Origins of social parasitism: the importance of divergence ages in phylogenetic studies,” Molecular Phylogenetics and Evolution, vol. 43, no. 3, pp. 1131–1137, 2007.
[10]
A. Buschinger, “Sympatric speciation and radiative evolution of socially parasitic ants—heretic hypotheses and their factual background,” Zeitschrift für Zoologische Systematik und Evolutionsforschung, vol. 28, no. 4, pp. 241–260, 1990.
[11]
K. Veps？l？inen, J. R. Ebsen, R. Savolainen, and J. J. Boomsma, “Genetic differentiation between the ant Myrmica rubra and its microgynous social parasite,” Insectes Sociaux, vol. 56, no. 4, pp. 425–437, 2009.
[12]
G. Jansen, R. Savolainen, and K. Veps？l？inen, “Phylogeny, divergence-time estimation, biogeography and social parasite-host relationships of the Holarctic ant genus Myrmica (Hymenoptera: Formicidae),” Molecular Phylogenetics and Evolution, vol. 56, no. 1, pp. 294–304, 2010.
[13]
R. R. Hora, C. Doums, C. Poteaux et al., “Small queens in the ant Ectatomma tuberculatum: a new case of social parasitism,” Behavioral Ecology and Sociobiology, vol. 59, no. 2, pp. 285–292, 2005.
[14]
J. P. Lachaud, A. Cadena, B. Schatz, G. Pérez-Lachaud, and G. Ibarra-Nú？ez, “Queen dimorphism and reproductive capacity in the ponerine ant, Ectatomma ruidum Roger,” Oecologia, vol. 120, no. 4, pp. 515–523, 1999.
[15]
J. C. Lenoir, J. P. Lachaud, A. Nettel, D. Fresneau, and C. Poteaux, “The role of microgynes in the reproductive strategy of the neotropical ant Ectatomma ruidum,” Naturwissenschaften, vol. 98, no. 4, pp. 347–356, 2011.
[16]
R. W. Howard and G. J. Blomquist, “Ecological, behavioral, and biochemical aspects of insect hydrocarbons,” Annual Review of Entomology, vol. 50, pp. 371–393, 2005.
[17]
P. D’Ettorre, “Multiple levels of recognition in ants: a feature of complex societies,” Biological Theory, vol. 3, no. 2, pp. 108–113, 2008.
[18]
A. Hefetz, “The evolution of hydrocarbon pheromone parsimony in ants (Hymenoptera: Formicidae)—interplay of colony odor uniformity and odor idiosyncrasy. A review,” Myrmecological News, vol. 10, pp. 59–68, 2007.
[19]
P. D’Ettorre and A. Lenoir, “Nestmate recognition,” in Ant Ecology, L. Lach, C. L. Parr, and K. L. Abbott, Eds., pp. 194–209, Oxford University Press, Oxford, UK, 2010.
[20]
C. Von Beeren, S. Pohl, and V. Witte, “On the use of adaptive resemblance terms in chemical ecology,” Psyche, vol. 2012, Article ID 635761, 7 pages, 2012.
[21]
K. Dettner and C. Liepert, “Chemical mimicry and camouflage,” Annual Review of Entomology, vol. 39, pp. 129–154, 1994.
[22]
A. Lenoir, P. D'Ettorre, C. Errard, and A. Hefetz, “Chemical ecology and social parasitism in ants,” Annual Review of Entomology, vol. 46, pp. 573–599, 2001.
[23]
T. Akino, “Chemical strategies to deal with ants: a review of mimicry, camouflage, propaganda, and phytomimesis by ants (Hymenoptera: Formicidae) and other arthropods,” Myrmecological News, vol. 11, pp. 173–181, 2008.
[24]
N. Franks, M. Blum, R. K. Smith, and A. B. Allies, “Behavior and chemical disguise of cuckoo ant Leptothorax kutteri in relation to its host Leptothorax acervorum,” Journal of Chemical Ecology, vol. 16, no. 5, pp. 1431–1444, 1990.
[25]
R. R. Hora, R. Blatrix, D. Fresneau, and R. Fénéron, “Social interactions between an inquiline ant, Ectatomma parasiticum, and its host, Ectatomma tuberculatum (Formicidae, Ectatomminae),” Journal of Ethology, vol. 27, no. 2, pp. 285–288, 2009.
[26]
R. M. Feitosa, R. R. Hora, J. H. C. Delabie, J. Valenzuela, and D. Fresneau, “A new social parasite in the ant genus Ectatomma F. Smith (Hymenoptera, Formicidae, Ectatomminae),” Zootaxa, no. 1713, pp. 47–52, 2008.
[27]
R. R. Da Hora, R. Fénéron, J. Valenzuela, M. E. Favila, and D. Fresneau, “Queen-size dimorphism in the ant Ectatomma tuberculatum (Hymenoptera: Formicidae: Ponerinae),” Sociobiology, vol. 38, no. 3, pp. 407–420, 2001.
[28]
F. Savarit and R. Fénéron, “Imperfect chemical mimicry explains the imperfect social integration of the inquiline ant, Ectatomma parasiticum,” in preparation.
[29]
C. G. Castillo, “Ecología del paisaje del municipio de jalcomulco,” in Faculdad de Ciencias, UNAM, Veracruz MSc, 1995.
[30]
E. Garcia, “Modificaciones al sistema de clasificación climática de K？ppen,” in Instituto de Geografía, Universidad Nacional Autónoma de México, México D.F., 1973.
[31]
R. H. Crozier and Y. C. Crozier, “The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization,” Genetics, vol. 133, no. 1, pp. 97–117, 1993.
[32]
J. D. Thompson, D. G. Higgins, and T. J. Gibson, “CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice,” Nucleic Acids Research, vol. 22, no. 22, pp. 4673–4680, 1994.
[33]
T. H. Jukes and C. R. Cantor, “Evolution of protein molecules,” in Mammalian Protein Metabolism, H. N. Munro, Ed., pp. 21–132, Academic Press, New York, NY, USA, 1969.
[34]
K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “Mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011.
[35]
R. Fénéron, “A new ethological test to study nestmate recognition in adult ants,” Insectes Sociaux, vol. 43, no. 2, pp. 131–135, 1996.
[36]
B. H？lldobler, C. Peeters, and M. Obermayer, “Exocrine glands and the attractiveness of the ergatoid queen in the ponerine ant Megaponera foetens,” Insectes Sociaux, vol. 41, no. 1, pp. 63–72, 1994.
[37]
N. A. Weber, “Two common ponerine ants of possible economic significance, Ectatomma tuberculatum (Olivier) and E. ruidum Roger,” Proceedings of the Entomological Society of Washington, vol. 48, no. 1, pp. 1–16, 1946.
[38]
G. Pérez-Lachaud, J. E. Valenzuela, and J.-P. Lachaud, “Is increased resistance to parasitism at the origin of polygyny in a mexican population of the ant Ectatomma tuberculatum (Hymenoptera: Formicidae)?” The Florida Entomologist, vol. 94, no. 3, pp. 677–684, 2011.
[39]
L. Keller, Ed., Queen Number and Sociality in Insects, Oxford University Press, Oxford, UK, 1993.
[40]
J. Heinze, “Social plasticity: ecology, genetics and the structure of ant societies,” in Ecology of Social Evolution, J. Korb and J. Heinze, Eds., pp. 129–150, Springer, Berlin, Germany, 2008.
[41]
L. Zinck, P. Jaisson, R. R. Hora, D. Denis, C. Poteaux, and C. Doums, “The role of breeding system on ant ecological dominance: genetic analysis of Ectatomma tuberculatum,” Behavioral Ecology, vol. 18, no. 4, pp. 701–708, 2007.
[42]
D. Leston, “A neotropical ant mosaic,” Annals of the Entomological Society of America, vol. 71, no. 4, pp. 649–653, 1978.
[43]
J. D. Majer, J. H. C. Delabie, and M. R. B. Smith, “Arboreal ant community patterns in Brazilian cocoa farms,” Biotropica, vol. 26, no. 1, pp. 73–83, 1994.
[44]
T. McGlynn, “Serial monodomy in the gypsy ant, Aphaenogaster araneoides: does nest odor reduction influence colony relocation?” Journal of Insect Science, vol. 10, article 195, 2010.
[45]
L. Keller, “Social life: the paradox of multiple-queen colonies,” Trends in Ecology and Evolution, vol. 10, no. 9, pp. 355–360, 1995.
[46]
P. Nonacs and J. E. Tobin, “Selfish larvae: development and the evolution of parasitic behavior in the Hymenoptera,” Evolution, vol. 46, no. 6, pp. 1605–1620, 1992.
[47]
S. Aron, L. Passera, and L. Keller, “Evolution of social parasitism in ants: size of sexuals, sex ratio and mechanisms of caste determination,” Proceedings of the Royal Society B, vol. 266, no. 1415, pp. 173–177, 1999.
[48]
D. Lambardi, F. R. Dani, S. Turillazzi, and J. J. Boomsma, “Chemical mimicry in an incipient leaf-cutting ant social parasite,” Behavioral Ecology and Sociobiology, vol. 61, no. 6, pp. 843–851, 2007.
[49]
S. Dronnet, X. Simon, J. C. Verhaeghe, P. Rasmont, and C. Errard, “Bumblebee inquilinism in Bombus (Fernaldaepsithyrus) sylvestris (Hymenoptera, Apidae): behavioural and chemical analyses of host-parasite interactions,” Apidologie, vol. 36, no. 1, pp. 59–70, 2005.
[50]
M. F. Sledge, F. R. Dani, R. Cervo, L. Dapporto, and S. Turillazzi, “Recognition of social parasites as nest-mates: adoption of colony-specific host cuticular odours by the paper wasp parasite Polistes sulcifer,” Proceedings of the Royal Society B, vol. 268, no. 1482, pp. 2253–2260, 2001.
[51]
C. W. Rettenmeyer, H. Topoff, and J. Mirenda, “Queen retinues of army ants (Hymenoptera, Formicidae, Ecitoninae),” Annals of the Entomological Society of America, vol. 71, no. 4, pp. 519–528, 1978.
[52]
K. N. Slessor, M. L. Winston, and Y. Le Conte, “Pheromone communication in the honeybee (Apis mellifera L.),” Journal of Chemical Ecology, vol. 31, no. 11, pp. 2731–2745, 2005.
[53]
T. Monnin, “Chemical recognition of reproductive status in social insects,” Annales Zoologici Fennici, vol. 43, no. 5-6, pp. 515–530, 2006.
[54]
L. Zinck, D. Denis, R. R. Hora et al., “Behavioral and chemical correlates of long-term queen adoption in the facultative polygynous ant Ectatomma tuberculatum,” Journal of Insect Behavior, vol. 22, no. 5, pp. 362–374, 2009.
[55]
R. R. Hora, A. Ionescu-Hirsh, T. Simon et al., “Postmating changes in cuticular chemistry and visual appearance in Ectatomma tuberculatum queens (Formicidae: Ectatomminae),” Naturwissenschaften, vol. 95, no. 1, pp. 55–60, 2008.
[56]
R. Fénéron, E. Nowbahari, and F. Dutrou, “Reconnaissance intercoloniale et niveau d’agression chez la fourmi Ponérine, Ectatomma tuberculatum,” Actes Colloques Insectes Sociaux, vol. 12, pp. 33–36, 1999.
[57]
R. H. Crozier and M. W. Dix, “Analysis of two genetic models for the innate components of colony odor in social Hymenoptera,” Behavioral Ecology and Sociobiology, vol. 4, no. 3, pp. 217–224, 1979.
[58]
L. Sundstr？m, “Queen acceptance and nestmate recognition in monogyne and polygyne colonies of the ant Formica truncorum,” Animal Behaviour, vol. 53, no. 3, pp. 499–510, 1997.
[59]
S. J. Martin, H. Helanter？, K. Kiss, Y. R. Lee, and F. P. Drijfhout, “Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants,” Insectes Sociaux, vol. 56, no. 4, pp. 375–383, 2009.
[60]
D. Moore and J. Liebig, “Mixed messages: fertility signaling interferes with nestmate recognition in the monogynous ant Camponotus floridanus,” Behavioral Ecology and Sociobiology, vol. 64, no. 6, pp. 1011–1018, 2010.
