Abstract
In the fungus-growing ant genus Atta, foundress queens nourish their brood and incipient fungus gardens with nutrients derived from trophic eggs. We discovered a third kind of egg laid by Atta foundresses in addition to reproductive and trophic eggs. We use fluorescent microscopy to show that this third type of eggs represents reproductive eggs that are unviable and fail to develop. Unviable reproductive eggs are somewhat larger (≈ 490 µm × 317 µm) than regular reproductive eggs (≈ 425 µm × 240 µm), but smaller than trophic eggs (≈ 640 µm × 530 µm). Trophic eggs liquify by some endogenous process within 24 h after oviposition to release nutrient contents. Unviable reproductive eggs do not liquify, but unviable reproductive eggs can be digested by the fungus, whereas reproductive eggs are not digested by the fungus to complete their development. We also report the first observation for A. texana of nanitic males (presumably diploid males) that were killed by the foundress queen shortly after the males’ eclosion.
References
Armitage S, Boomsma J, Baer B (2010) Diploid male production in a leaf-cutting ant. Ecol Entomol 35:175–182
Augustin JO, Santos JFL, Elliot SL (2011) A behavioral repertoire of Atta sexdens (Hymenoptera, Formicidae) queens during the claustral founding and ergonomic stages. Insect Soc 58:197–206
Autuori M (1942) Contribuição para o conhecimento da saúva (Atta spp. - Hymenoptera: Formicidae). II. O sauveiro inicial (Atta sexdens rubropilosa Forel, 1908). Arq Inst Biol 13:67–86
Bazire-Bénazet M (1957) Sur la formation de l’oeuf alimentaire chez Atta sexdens rubropilosa, Forel, 1908 (Hym., Formicidae). Comptes Rendus de l’Académie des Sciences 244:1277–1280
Brown MJF, Bonhoeffer S (2003) On the evolution of claustral colony founding in ants. Evol Ecol Res 5:305–313
Camargo RS, Silva EJ, Forti LC, de Matos CAO (2016) Initial development and production of CO2 in colonies of the leaf-cutting ant Atta sexdens during the claustral foundation. Sociobiology 63:720–723
Della Lucia TMC, Moreira DDO, Oliveira MA, Araújo MS (1995) Perdas de peso de rainha de Atta durante a fundação e o estabelecimento das colônias. Rev Bras Biol 55:336–533
Diehl-Fleig E, de Araújo AM (1996) Haplometrosis and pleometrosis in the ant Acromyrmex striatus (Hymenoptera: Formicidae). Insect Soc 43:47–51
Dijkstra MB, Nash DR, Boomsma JJ (2005) Self-restraint and sterility in workers of Acromyrmex and Atta leafcutter ants. Insect Soc 52:67–76
Duchateau MJ, Marien J (1995) Sexual biology of haploid and diploid males in the bumble bee Bombus terrestris. Insect Soc 42:255–266
Fang CC (2019) Embryogenesis, trophic eggs, and early colony growth of myrmicine ants. Dissertation, The University of Texas at Austin
Fang CC, Rajakumar A, Abouheif E, Kenny A, Mueller UG, Stein D. Embryogenesis in myrmicine ants exhibits features of both short and long derm-band development (in preparation)
Fernández-Marín H, Wcislo WT (2005) Production of minima workers by gynes of Atta colombica Guérin-Ménéville (Hymenoptera: Formicidae; Attini) that lack a fungal pellet. J Kans Entomol Soc 78:290–292
Fernández-Marín H, Zimmerman JK, Wcislo WT, Rehner SA (2005) Colony foundation, nest architecture and demography of a basal fungus-growing ant, Mycocepurus smithii (Hymenoptera, Formicidae). J Nat Hist 39:1735–1743
Fujihara RT, Camargo RS, Forti LC (2012) Lipid and energy contents in the bodies of Atta sexdens rubropilosa Forel 1908 (Hymenoptera: Formicidae) queens: pre-and post-nuptial flight. Rev Bras Entomol 56:73–75
Gerloff CU, Ottmer BK, Schmid Hempel P (2003) Effects of inbreeding on immune response and body size in a social insect Bombus terrestris. Funct Ecol 17:582–589
Glancey BM, Stringer CE, Bishop PM (1973) Trophic egg production in the imported fire ant, Solenopsis invicta. J Ga Entomol Soc 8:217–220
Gobin B, Peeters C, Billen J (1998) Production of trophic eggs by virgin workers in the ponerine ant Gnamptogenys menadensis. Physiol Entomol 23:329–336
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Boston
Hölldobler B, Wilson EO (2010) The leafcutter ants. Harvard University Press, Boston
Huber J (1905) Über die Koloniegründung bei Atta sexdens. Biologisches Centralblatt 25(606–619):625–635
Huber J (1907) The founding of colonies by Atta sexdens. In: Smithson Report for 1906:355–372 [this is a translation of Huber 1905]
Lee CC, Nakao H, Tseng SP, Hsu HW, Lin GL, Tay JW, Billen J, Ito F, Lee CY, Lin CC, Yang CCS (2017) Worker reproduction of the invasive yellow crazy ant Anoplolepis gracilipes. Front Zool 14:24
Marti HE, Carlson AL, Brown BV, Mueller UG (2015) Foundress queen mo rtality and early colony growth of the leafcutter ant, Atta texana (Formicidae, Hymenoptera). Insect Soc 62:357–363
Mehidabadi NJ, Schultz TR (2009) Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini). Myrmecol News 13:37–55
Mueller UG (2002) Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis. Am Nat 160:S67–S98
Mueller UG, Rehner SA, Schultz TR (1998) The evolution of agriculture in ants. Science 281:2034–2038
Mueller UG, Schultz TR, Currie CR, Adams RMM, Malloch D (2001) The origin of the attine ant-fungus mutualism. Q Rev Biol 76:169–197
Mueller UG, Ishak HD, Bruschi SM, Smith CC, Herman JJ, Solomon SE, Mikheyev AS, Rabeling C, Scott JJ, Cooper M, Rodrigues A, Ortiz A, Brandão CRF, Lattke JE, Pagnocca FC, Rehner SA, Schultz TR, Vasconcelos HL, Adams RMM, Bollazzi M, Clark RM, Himler AG, LaPolla JS, Leal IR, Johnson RA, Roces F, Sosa-Calvo J, Wirth R, Bacci M Jr (2017) Biogeography of mutualistic fungi cultivated by leafcutter ants. Mol Ecol 26:6921–6937
Mueller UG, Kardish MR, Ishak HD, Wright AM, Solomon SE, Bruschi SM, Carlson AL, Bacci M Jr (2018) Phylogenetic patterns of ant-fungus associations indicate that farming strategies, not only a superior fungal cultivar, explain the ecological success of leafcutter ants. Mol Ecol 27:2414–2434
Peeters C (2017) Independent colony foundation in Paraponera clavata (Hymenoptera: Formicidae): first workers lay trophic eggs to feed queen’s larvae. Sociobiology 64:417–422
Peeters C, Ito F (2001) Colony dispersal and the evolution of queen morphology in social Hymenoptera. Ann Rev Entomol 46:601–630
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 01 Mar 2019
Ross KG, Fletcher DJC (1985) Genetic origin of male diploidy in the fire ant Solenopsis invicta (Hymenoptera, Formicidae) and its evolutionary significance. Evolution 39:888–903
Seal JN (2009) Scaling of body weight and fat content in fungus-gardening ant queens: does this explain why leaf-cutting ants found claustrally? Insect Soc 56:135–141
Verza SS, Mussury RM, Camargo RS, Andrade APP, Forti LC (2017) Oviposition, life cycle, and longevity of the leaf-cutting ant Acromyrmex rugosus rugosus. Insects 8:80
von Ihering H (1898) Die Anlagen neuer Colonien und Pilzgärten bei Atta sexdens. Zool Anzeiger 21:238–245
Weber NA (1958) Evolution in fungus-growing ants. Proc Tenth Int Congress Entomol 2:459–473
Weber NA (1972) Gardening ants, the attines. The American Philosophical Society, Philadelphia
Wheeler W (1907) The fungus-growing ants of north America. Bull Am Mus Nat Hist 23:669–807
Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge
Acknowledgements
We thank Zach Phillips, Emma Dietrich, Yao-Lun Yang for ant collection; and Ryan Bailey for colony maintenance. The study was funded by a Texas Ecolab award to CCF, a National Science Foundation award DEB-1354666 to UGM, and the W.M. Wheeler Lost Pines Endowment from the University of Texas at Austin.
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Fang, CC., Mueller, U.G. A new type of egg produced by foundress queens of Atta texana (Attini, Formicidae). Insect. Soc. 66, 601–609 (2019). https://doi.org/10.1007/s00040-019-00724-w
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DOI: https://doi.org/10.1007/s00040-019-00724-w