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Acromyrmex charruanus: a new inquiline social parasite species of leaf-cutting ants

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Abstract

Social parasites exploit the colony resources of social species to secure their own survival and reproduction. Social parasites are frequently studied as models for conflict and cooperation as well as for speciation. The eusocial Hymenoptera harbor a diverse array of socially parasitic species with idiosyncratic life history strategies, but it is probably in the ants where social parasites are most speciose and have evolved the highest degrees of morphological and behavioral specialization. In the fungus-growing ants, a total of five obligate social parasites are known: four species are parasites of leaf-cutting ants and one species parasitizes a primitive fungus-growing ant species in the genus Mycocepurus. Here we describe a new species of socially parasitic leaf-cutting ant, Acromyrmex charruanus sp. nov., from Uruguay, and we report initial observations on the parasite’s life history as well as on the morphological and behavioral adaptations related to the inquiline syndrome. Our observations suggest that Acromyrmex charruanus is an obligate inquiline social parasite of the thatch-mound-building, leaf-cutting ant Acromyrmex heyeri. Acromyrmex charruanus appears to be tolerant of the host, producing sexual offspring in the presence of the A. heyeri host queen. Queens of A. charruanus appear to reproduce semelparously and sexual offspring are produced during the austral fall (February), which differs significantly from the mating biology of the host species, which reproduces during the southern-hemisphere spring (October–December). We suggest that the diametrically opposed mating seasons of parasite and host might be adaptive, allowing the parasite to avoid competition for resources with the host sexual brood. The morphological and behavioral adaptations of A. charruanus accord with characters observed to arise early during the evolution of other ant inquiline parasite species, and so far we have no evidence for the existence of a worker caste in A. charruanus. Further field studies and behavioral experiments need to confirm our first observations and explore A. charruanus’s behavioral ecology, evolution, and life history in more detail.

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References

  • Baer B, Boomsma JJ (2006) Mating biology of the leaf-cutting ants Atta colombica and A. cephalotes. J Morphol 267:1165–1171

    Article  PubMed  Google Scholar 

  • Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352

    Article  Google Scholar 

  • Bekkevold D, Boomsma JJ (2000) Evolutionary transition to a semelparous life history in the socially parasitic ant Acromyrmex insinuator. J Evol Biol 13:615–623

    Article  Google Scholar 

  • Bekkevold D, Frydenberg J, Boomsma JJ (1999) Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior. Behav Ecol Sociobiol 46:103–109

    Article  Google Scholar 

  • Bollazzi M, Roces F (2010a) Leaf-cutting ant workers (Acromyrmex heyeri) trade off nest thermoregulation for humidity control. J Ethol 28:399–403

    Article  Google Scholar 

  • Bollazzi M, Roces F (2010b) The thermoregulatory function of thatched nests in the South American grass-cutting ant, Acromyrmex heyeri. J Insect Sci 10(137):1–17

    Article  Google Scholar 

  • Bollazzi M, Kronenbitter J, Roces F (2008) Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants. Oecologia 158:165–175

    Article  PubMed  Google Scholar 

  • Bolton B (2014) An online catalog of the ants of the world. http://antcat.org. Accessed 26 Sept 2014

  • Bonetto AA (1959) Las hormigas “cortadoras” de la Provincia de Santa Fé (generos: Atta y Acromyrmex). Ministerio de Agricultura y Ganadería (Dirección General de Recurzos Naturales), Santa Fé, Argentina, p 79

  • Boomsma JJ, Nash D (2014) Evolution: sympatric speciation the eusocial way. Curr Biol 24:R798–R800

    Article  CAS  PubMed  Google Scholar 

  • Boomsma JJ, Huszár DB, Pedersen JS (2014) The evolution of multiqueen breeding in eusocial lineages with permanent physically differentiated castes. Anim Behav 92:241–252

    Article  Google Scholar 

  • Bourke AFG, Franks NR (1991) Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants. Biol J Linn Soc 43:157–178

    Article  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton

    Google Scholar 

  • Brandão CRF (1991) Adendos ao catálogo abreviado das formigas da região Neotropical (Hymenoptera: Formicidae). Rev Brasil Entomol 35:319–412

    Google Scholar 

  • Brown WL Jr (1973) A comparison of the Hylean and Congo-West African rain forest ant faunas. In: Meggers BJ, Ayensu ES, Duckworth WD (eds) Tropical forest ecosystems in Africa and South America: a comparative review. Smithsonian Institution Press, Washington DC, pp 161–185

    Google Scholar 

  • Bruch C (1928) Estudios mirmecológicos. Anales del Museo Nacional de Historia Natural Buenos Aires 34:341–360

    Google Scholar 

  • Bueno OC, Hebling MJ, Schneider MO, Pagnocca FC, Bacci JRM (2002) Occurrence of winged forms of Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae) in laboratory colonies. Neotrop Entomol 31:469–473

    Article  Google Scholar 

  • Buschinger A (1986) Evolution of social parasitism in ants. Trends Ecol Evol 1:155–160

    Article  CAS  PubMed  Google Scholar 

  • Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235

    Google Scholar 

  • Buschinger A, Klump B (1988) Novel strategy of host-colony exploitation in a permanently parasitic ant, Doronomyrmex goesswaldi. Naturwissenschaften 75:577–578

    Article  Google Scholar 

  • Cabrera AL, Willink A (1980) Biogeografía de América Latina. Segunda edición. Monografía 13, serie biología. Programa Regional de Desarrollo Científico y Tecnológico, Organización de los Estados Americanos, p 122

  • Caldera E, Poulsen M, Suen G, Currie CR (2009) Insect symbioses—a case study of past, present, and future fungus-growing ant research. Environ Entomol 38:78–92

    Article  PubMed  Google Scholar 

  • Calero-Torralbo M, Valera F (2008) Synchronization of host-parasite cycles by means of diapause: host influence and parasite response to involuntary host shifting. Parasitology 135:1343–1352

    Article  CAS  PubMed  Google Scholar 

  • Cristiano MP, Cardoso DC, Fernandes-Salomão TM (2013) Cytogenetic and molecular analyses reveal a divergence between Acromyrmex striatus (Roger, 1863) and other congeneric species: taxonomic implications. PLoS One 8:e59784

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Souza DJ, Lino Neto J, Della Lucia TMC, Peternelli EF (2004) Occurrence of polygyny in Acromyrmex subterraneus molestans Santschi 1925 (Hymenoptera: Formicidae). Ciência Rural 34:1611–1613

    Article  Google Scholar 

  • De Souza DJ, Soares I, Della Lucia TMC (2007) Acromyrmex ameliae sp. n. (Hymenoptera: Formicidae): a new social parasite of leaf-cutting ants in Brazil. Insect Sci 14:251–257

    Article  Google Scholar 

  • DeHeer CJ, Tschinkel WR (1998) The success of alternative reproductive tactics in monogyne populations of the ant Solenopsis invicta: significance for transitions in social organization. Behav Ecol 9:130–135

    Article  Google Scholar 

  • Delabie JHC (1989) Observações sobre a ocorrência de poliginia em colônias de Acromyrmex subterraneus brunneus Forel 1893, em cacauais (Formicidae, Myrmicinae, Attini). Anais da Sociedade Entomolocica do Brasil 18:193–197

    Google Scholar 

  • Delabie JHC, Fowler HG, Schlindwein MN (1993) Ocorrência do parasita social Pseudoatta sp. nova em ninhos de Acromyrmex rugosus em Ilhéus, Bahia: primeiro registro para os trópicos. Paper presented at the IV International Symposium on Pest Ants and XI Encontro de Mirmecologia, Belo Horizonte, Minas Gerais, Brazil

  • Della Lucia TMC (2011) Formigas Cortadeiras: da Bioecologia ao Manejo. Editora da UFV, Viçosa

    Google Scholar 

  • Della Lucia TMC, Vilela EF (1986) Ocorrencia de poligina em Acromyrmex subterraneus Forel, 1893 (Hymenoptera: Formicidae). Anais da Sociedade Entomolocica do Brasil 15:377–378

    Google Scholar 

  • Diehl E, de Araujjo AM, Cavalli-Molina S (2001) Genetic variability and social structure of colonies in Acromyrmex heyeri and A. striatus (Hymenoptera: Formicidae). Brazil J Biol 61:667–678

    CAS  Google Scholar 

  • Diehl-Fleig E (1993) Sex ratio and nuptial flight pattern of the leaf-cutting ants Acromyrmex heyeri and A. striatus (Hymenoptera: Formicidae). Insect Soc 40:111–113

    Article  Google Scholar 

  • Dijkstra MB, Boomsma JJ (2006) Are workers of Atta leafcutter ants capable of reproduction? Insect Soc 53:136–140

    Article  Google Scholar 

  • Elmes GW (1973) Observations on the density of queens in natural colonies of Myrmica rubra L. (Hymenoptera: Formicidae). J Anim Ecol 42:761–771

    Article  Google Scholar 

  • Emery C (1905) Revisione delle specie del genere Atta appartenenti ai sottogeneri Moellerius e Acromyrmex. Memorie della R. Accademia delle Scienze dell’Istituto di Bologna 2:1–18

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Fowler HG (1981) On the emigration of leaf-cutting ant colonies. Biotropica 13:316

    Article  Google Scholar 

  • Gallardo A (1916) Notes systématiques et éthologiques sur les fourmis attines de la République Argentine. Anales del Museo Nacional de Historia Natural Buenos Aires 28:317–344

    Google Scholar 

  • Gallardo A (1929) Note sur les moeurs de la fourmi Pseudoatta argentina. Revista de la Sociedad Entomológica Argentina 2:197–202

    Google Scholar 

  • Gonçalves CR (1961) O género Acromyrmex no Brasil (Hym. Formicidae). Studia Entomologica 4:113–180

    Google Scholar 

  • Gotwald WH (1969) Comparative morphological studies of the ants, with particular reference to the mouthparts (Hymenoptera: Formicidae). Memoirs of the Cornell University Agricultural Experiment Station 408:1–150

    Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Hölldobler B, Wilson EO (2010) The leafcutter ants—civilization by instinct. W. W. Norton & Company, New York

    Google Scholar 

  • Jansen G, Savolainen R, Vepsäläinen K (2010) Phylogeny, divergence-time estimation, biogeography and social parasite–host relationships of the Holarctic ant genus Myrmica (Hymenoptera: Formicidae). Mol Phylog Evol 56:294–304

    Article  Google Scholar 

  • Johnson RA, Rissing SW (1993) Breeding biology of the desert leaf-cutter ant Acromyrmex versicolor (Pergande) (Hymenoptera: Formicidae). J Kansas Entomol Soc 66:127–128

    Google Scholar 

  • Jutsum AR, Cherrett JM (1977) Sexuals and a microgyne of Atta cephalotes (L.) (Hymenoptera, Formicidae) from laboratory cultures. Entomol Mon Mag 113:97–98

    Google Scholar 

  • Kempf W (1956) A morphological study on the male genitalia of Paracryptocerus (P.) pusillus (Hymenoptera: Formicidae). Rev Brasil Entomol 5:101–110

    Google Scholar 

  • Kempf WW (1972) Catálogo abreviado das formigas da região Neotropical. Studia Entomologica 15:3–344

    Google Scholar 

  • Klingenberg C, Brandão CRF (2009) Revision of the fungus-growing ant genera Mycetophylax Emery and Paramycetophylax Kusnezov rev. stat., and description of Kalathomyrmex n. gen. (Formicidae: Myrmicinae: Attini). Zootaxa 2052:1–31

    Google Scholar 

  • Kusnezov N (1954) Phyletische Bedeutung der Maxillar- und Labialtaster der Ameisen. Zool Anzeig 153:28–38

    Google Scholar 

  • Kutter H (1950) Über eine neue, extrem parasitische Ameise. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 23:81–94

    Google Scholar 

  • Kutter H (1969) Die sozialparasitischen Ameisen der Schweiz. Neujahrsblatt der Naturforschenden Gesellschaft in Zürich 171:1–62

    Google Scholar 

  • Lambardi D, Dani FR, Turillazzi S, Boomsma JJ (2007) Chemical mimicry in an incipient leaf-cutting ant social parasite. Behav Ecol Sociobiol 61:843–851

    Article  Google Scholar 

  • Mayhé-Nunes AJ (1995) Filogenia de los Attini (Hym., Formicidae): un aporte al conocimiento de las hormigas fungívoras. Universidad Simón Bolívar, Caracas, Venezuela, p 274

  • Mayhé-Nunes AJ, Jaffé K (1998) On the biogeography of Attini (Hymenoptera: Formicidae). Ecotropicos 11:45–54

    Google Scholar 

  • Möller A (1893) Die Pilzgärten einiger Südamerikanischer Ameisen. Botanische Mittheilungen aus den Tropen 6:1–142

    Google Scholar 

  • Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Ann Rev Ecol Evol Syst 36:563–595

    Article  Google Scholar 

  • Nash DR, Boomsma JJ (2008) Communication between hosts and social parasites. In: Hughes DP, D’Ettorre P (eds) Sociobiology of communication: an interdisciplinary perspective. Oxford University Press, Oxford, pp 55–79

    Chapter  Google Scholar 

  • Nickele MA, Pie MR, Reis Filho W (2012) Emigration of a colony of the leaf-cutting ant Acromyrmex heyeri Forel (Hymenoptera, Formicidae). Rev Brasil Entomol 56:385–386

    Article  Google Scholar 

  • Nonacs P, Tobin JE (1992) Selfish larvae: development and the evolution of parasitic behavior in the Hymenoptera. Evolution 46:1605–1620

    Article  Google Scholar 

  • Overbeck GE, Müller SC, Fidelis A, Pfadenhauer J, Pillar VD, Blanco CC, Boldrini II, Both R, Forneck ED (2007) Brazil’s neglected biome: the South Brazilian Campos. Perspect Plant Ecol Evol Syst 9:101–116

    Article  Google Scholar 

  • Pagnocca FC, Masiulionis VE, Rodrigues A (2012) Specialized fungal parasites and opportunistic fungi in gardens of attine ants. Psyche J Entomol. doi:10.1155/2012/905109 Article ID 905109, p 9

    Google Scholar 

  • Rabeling C, Bacci M (2010) A new workerless inquiline in the Lower Attini (Hymenoptera: Formicidae), with a discussion of social parasitism in fungus-growing ants. Syst Entomol 35:379–392

    Article  Google Scholar 

  • Rabeling C, Cover SP, Johnson RA, Mueller UG (2007a) A review of the North American species of the fungus-gardening ant genus Trachymyrmex (Hymenoptera : Formicidae). Zootaxa 1664:1–53

    Google Scholar 

  • Rabeling C, Verhaagh M, Engels W (2007b) Comparative study of nest architecture and colony structure of the fungus-growing ants, Mycocepurus goeldii and M. smithii. J Insect Sci 7(40):1–13

    Article  Google Scholar 

  • Rabeling C, Bollazzi M, Bacci M Jr, Beasley RR, Lance SL, Jones KL, Pierce NE (2014a) Development and characterization of twenty-two polymorphic microsatellite markers for the leafcutter ant, Acromyrmex lundii, utilizing Illumina sequencing. Con Gen Res 6:319–322

    Article  Google Scholar 

  • Rabeling C, Schultz TR, Pierce NE, Bacci M Jr (2014b) A social parasite evolved reproductive isolation from its fungus-growing ant host in sympatry. Curr Biol 24:2047–2052

    Article  CAS  PubMed  Google Scholar 

  • Santschi F (1925) Revision du genre Acromyrmex Mayr. Rev Suisse Zool 31:355–398

    Google Scholar 

  • Savolainen R, Vepsäläinen K (2003) Sympatric speciation through intraspecific social parasitism. Proc Natl Acad Sci USA 100:7169–7174

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schär S, Nash DR (2014) Evidence that microgynes of Myrmica rubra ants are social parasites that attack old host colonies. J Evol Biol 27:2396–2407

    Article  PubMed  Google Scholar 

  • Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, New York

    Google Scholar 

  • Schultz TR (2007) The fungus-growing ant genus Apterostigma in Dominican amber. Mem Am Entomol Inst 80:425–436

    Google Scholar 

  • Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schultz TR, Meier R (1995) A phylogenetic analysis of the fungus-growing ants (Hymenoptera: Formicidae: Attini) based on morphological characters of the larvae. Syst Entomol 20:337–370

    Article  Google Scholar 

  • Schultz TR, Bekkevold D, Boomsma JJ (1998) Acromyrmex insinuator new species: an incipient social parasite of fungus-growing ants. Insect Soc 45:457–471

    Article  Google Scholar 

  • Schultz TR, Mueller UG, Currie CR, Rehner SA (2005) Reciprocal illumination: a comparison of agriculture in humans and ants. In: Vega F, Blackwell M (eds) Ecological and evolutionary advances in insect-fungal associations. Oxford University Press, New York, pp 149–190

    Google Scholar 

  • Seifert B (2010) Intranidal mating, gyne polymorphism, polygyny, and supercoloniality as factors for sympatric and parapatric speciation in ants. Ecol Entomol 35:33–40

    Article  Google Scholar 

  • Seppä P (1994) Sociogenetic organization of the ants Myrmica ruginodis and Myrmica lobicornis: number, relatedness and longevity of reproducing individuals. J Evol Biol 7:71–95

    Article  Google Scholar 

  • Sosa-Calvo J, Schultz TR, Brandão CR, Klingenberg C, Feitosa RM, Rabeling C, Bacci M Jr, Lopes CT, Vasconcelos HL (2013) Cyatta abscondita: taxonomy, evolution, and natural history of a new fungus-farming ant genus from Brazil. PLoS One 8(11):e80498

    Article  PubMed Central  PubMed  Google Scholar 

  • Sumner S, Hughes WOH, Boomsma JJ (2003a) Evidence for differential selection and potential adaptive evolution in the worker caste of an inquiline social parasite. Behav Ecol Sociobiol 54:256–263

    Article  Google Scholar 

  • Sumner S, Nash DR, Boomsma JJ (2003b) The adaptive significance of inquiline parasite workers. Proc R Soc Lond Ser B Biol Sci 270:1315–1322

    Article  Google Scholar 

  • Sumner S, Aanen DK, Delabie J, Boomsma JJ (2004) The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule. Insect Soc 51:37–42

    Article  Google Scholar 

  • Tschinkel WR (1996) A newly-discovered mode of colony founding among fire ants. Insect Soc 43:267–276

    Article  Google Scholar 

  • Wcislo WT (1987) The roles of seasonality, host synchrony, and behaviour in the evolutions and distributions of nest parasites in Hymenoptera (Insecta), with special reference to bees (Apoidea). Biol Rev 62:515–542

    Article  Google Scholar 

  • Weber N (1957) Dry season adaptations of fungus-growing ants and their fungi. Anat Rec 128:638

    Google Scholar 

  • Weber NA (1972) Gardening ants: the Attines. Memoirs of the American Philosophical Society, Philadelphia

    Google Scholar 

  • Wheeler WM (1907) The fungus-growing ants of North America. Bull Am Mus Nat Hist 23:669–807

    Google Scholar 

  • Wilson EO (1971) The Insect Societies. Harvard University Press, Cambridge

    Google Scholar 

  • Wilson EO (1984) Tropical social parasites in the ant genus Pheidole, with an analysis of the anatomical parasitic syndrome (Hymenoptera: Formicidae). Insect Soc 31:316–334

    Article  Google Scholar 

  • Yek SH, Boomsma JJ, Poulsen M (2012) Towards a better understanding of the evolution of specialized parasites of fungus-growing ant crops. Psyche. doi:10.1155/2012/239392 Article ID 239392, p 10

    Google Scholar 

  • Zolessi LC, Abenante YP (1974) Nidificación y mesoetología de Acromyrmex en el Uruguay III. Acromyrmex (A.) hispidus Santschi, 1925 (Hymenoptera: Formicidae). Revista de Biología del Uruguay 1:151–165

    Google Scholar 

  • Zolessi LC, González LA (1974) Nidificación y mesoetología de Acromyrmex en el Uruguay, II. Acromyrmex (Acromyrmex) lobicornis (Emery, 1887) (Hymenoptera: Formicidae). Revista de Biología del Uruguay 2:37–57

    Google Scholar 

  • Zolessi LC, González LA (1979) Observaciones sobre el género Acromyrmex en el Uruguay IV. A. (Acromyrmex) lundi (Guérin, 1838) (Hymenoptera: Formicidae). Revista de la Facultad de Humanidades y Ciencias Serie Ciencias Biologicas 1:9–28

    Google Scholar 

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Acknowledgments

We gratefully acknowledge the Dirección General de Recursos Naturales Renovables for permission to conduct fieldwork in Uruguay. We thank Naomi Pierce for permission to conduct parts of this study in her laboratory at Harvard University. Sarah Callan and Amelia Harvey kindly assisted in the laboratory. Christian Rabeling was supported by the National Science Foundation (DEB-1456964), the Harvard Society of Fellows, and by the William F. Milton Fund from the Harvard Medical School. Ted Schultz was supported by the National Science Foundation (DEB-0949689, DEB-1456964) and the Smithsonian Competitive Grants Program for Science. Maurício Bacci Jr. acknowledges support from FAPSP (2011/50226-0) and CNPq (311562/2012-4 and 487639/2012-0). Martin Bollazzi is grateful to Daniel Ramírez from Cambium Forestal for facilitating access to field research sites.

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Rabeling, C., Schultz, T.R., Bacci, M. et al. Acromyrmex charruanus: a new inquiline social parasite species of leaf-cutting ants. Insect. Soc. 62, 335–349 (2015). https://doi.org/10.1007/s00040-015-0406-6

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