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Mechanism of facultative parthenogenesis in the ant Platythyrea punctata

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Abstract

Thelytokous parthenogenesis, the production of diploid female offspring from unfertilized eggs, can be caused by several cytological mechanisms, which have a different impact on the genetic variation on the offspring. The ponerine ant Platythyrea punctata is widely distributed throughout the Caribbean Islands and Central America and exhibits facultative parthenogenesis. Workers in many field colonies from the Caribbean Islands have identical multilocus genotypes and are thus probably clonal, but the occurrence of males makes an ameiotic mechanism of thelytoky unlikely. To clarify the details of thelytoky in this species we compared the multilocus genotypes of mothers and their offspring in experimental colonies and analyzed the genotypes of haploid and diploid males. Additionally, we screened a large number of field colonies from thelytokous populations for the occurrence of recombination events. According to these data, automixis with central fusion and a reduced recombination rate is the most likely mechanism of thelytoky, as in the Cape honeybee and the ant Cataglyphis cursor.

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References

  • Balloux F, Lehmann L, de Meeûs T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164:1635–1644

    PubMed  Google Scholar 

  • Baudry E, Kryger P, Allsopp M, Koeniger N, Vautrin D, Mougel F, Cornuet J-M, Solignac M (2004) Whole genome scan in thelytokous-laying workers of the Cape honeybee (Apis mellifera capensis): central fusion, reduced recombination rates and centromer mapping using half-tetrad analysis. Genetics 167:243–252

    Article  CAS  PubMed  Google Scholar 

  • Belshaw R, Quicke DLJ (2003) The cytogenetics of thelytoky in a predominantly asexual parasitoid wasp with covert sex. Genome 46:170–173

    Article  PubMed  Google Scholar 

  • Bourtzis K, O’Neill S (1998) Wolbachia infections and arthropod reproduction. Bioscience 48:287–293

    Article  Google Scholar 

  • Cagniant H (1983) La parthénogenèse thélytoque et arrhénotoque des ouvrières de la fourmi Cataglyphis cursor Fonscolombe (Hyménoptères Formicidae). Étude biométrique des ouvrières et de leurs potentialités reproductrices. Insect Soc 30:241–254

    Article  Google Scholar 

  • Cook JM (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435

    Article  Google Scholar 

  • Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286

    Article  Google Scholar 

  • Fernández-Marín H, Zimmermann 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

    Article  Google Scholar 

  • Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, Keller L (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1235

    Article  CAS  PubMed  Google Scholar 

  • Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. P Natl Acad Sci USA 100:12836–12840

    Article  CAS  Google Scholar 

  • Hartmann A, Wantia J, Heinze J (2005) Facultative sexual reproduction in the parthenogenetic ant Platythyrea punctata. Insect Soc 52:155–162

    Article  Google Scholar 

  • Heinze J (2008) The demise of the standard ant. Myrmecol News 11:9–20

    Google Scholar 

  • Heinze J, Hölldobler B (1995) Thelytokous parthenogenesis and dominance hierarchies in the ponerine ant, Platythyrea punctata. Naturwissenschaften 82:40–41

    CAS  Google Scholar 

  • Himler AG, Caldera EJ, Baer B, Fernández-Marín H, Mueller UG (2009) No sex in fungus-farming ants or their crops. P Roy Soc Lond B Bio 276:2611–2616

    Article  Google Scholar 

  • Kellner K, Barth B, Heinze J (2010) Colony fusion causes within-colony variation in a parthenogenetic ant. Behav Ecol Sociobiol 64:737–746

    Google Scholar 

  • Lamb RY, Willey RB (1987) Cytological mechanisms of thelytokous parthenogenesis in insects. Genome 29:367–369

    Google Scholar 

  • Lattorff HMG, Moritz RFA, Fuchs S (2005) A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94:533–537

    Article  CAS  PubMed  Google Scholar 

  • Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292–295

    Article  CAS  PubMed  Google Scholar 

  • Normark BB (2003) The evolution of alternative genetic systems in insects. Annu Rev Entomol 48:397–423

    Article  CAS  PubMed  Google Scholar 

  • Ohkawara K, Nakayama M, Satoh A, Trindl A, Heinze J (2006) Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol Lett 2:359–363

    Article  PubMed  Google Scholar 

  • Oldroyd BP, Allsopp MH, Gloag RS, Lim J, Jordan LA, Beekman M (2008) Thelytokous parthenogenesis in unmated queen honeybees (Apis mellifera capensis): Central fusion and high recombination rates. Genetics 180:359–366

    Article  PubMed  Google Scholar 

  • Pearcy M, Aron S, Doums C, Keller L (2004) Conditional use of sex and parthenogenesis for workers and queens in ants. Science 306:1780–1782

    Article  CAS  PubMed  Google Scholar 

  • Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382

    Article  CAS  PubMed  Google Scholar 

  • Pearcy M, Timmermans I, Allard D, Aron S (2009) Multiple mating in the ant Cataglyphis cursor: testing sperm limitation and the diploid male load hypotheses. Insect Soc 56:94–102

    Article  Google Scholar 

  • Rabeling C, Lino-Neto J, Capellari SC, Dos-Santos IA, Mueller UG (2009) Thelytokous parthenogenesis in the fungus-gardening ant Mycocepurus smithii (Hymenoptera: Formicicdae). PLoS ONE 4:e6781

    Article  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Preparation and analysis of eukaryotic genomic DNA. In: Sambrook J, Russell DW (eds) Molecular cloning: a laboratory manual. Harbor Laboratory Press, Cold Spring Harbor, New York, pp 23–25

    Google Scholar 

  • Schilder K (1999) “Safer without sex?” Thelytokous parthenogenesis and regulation of reproduction in the ant Platythyrea punctata. Dissertation, Julius-Maximilans-Universität, Würzburg

  • Schilder K, Heinze J, Hölldobler B (1999a) Colony structure and reproduction in the thelytokous parthenogenetic ant Platythyrea punctata (F Smith) (Hymenoptera, Formicidae). Insect Soc 46:150–158

    Article  Google Scholar 

  • Schilder K, Heinze J, Roy G, Hölldobler B (1999b) Microsatellites reveal clonal structure of populations of the thelytokous parthenogenetic ant Platythyrea punctata (F Smith) (Hymenoptera: Formicidae). Mol Ecol 8:1497–1507

    Article  PubMed  Google Scholar 

  • Slobodchikoff CN, Daly HV (1971) Systematic and evolutionary implications of parthenogenesis in the Hymenoptera. Am Zool 11:273–282

    Google Scholar 

  • Stouthamer R, Kazmer DJ (1994) Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73:317–327

    Article  Google Scholar 

  • Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton

    Google Scholar 

  • Tsuji K (1988) Obligate parthenogenesis and reproductive division of labor in the Japanese queenless ant Pristomyrmex pungens. Behav Ecol Sociobiol 23:247–255

    Article  Google Scholar 

  • Tsuji K, Yamauchi K (1995) Production of females by parthenogenesis in the ant Cerapachys biroi. Insect Soc 42:333–336

    Article  Google Scholar 

  • van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1

    Article  PubMed  Google Scholar 

  • Verma LR, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the Cape honeybee (Apis mellifera capensis Escholtz). Apidologie 14:47–57

    Article  Google Scholar 

  • Wenseleers T, Billen J (2000) No evidence for Wolbachia-induced parthenogenesis in the social Hymenoptera. J Evolution Biol 13:277–280

    Article  Google Scholar 

  • Wenseleers T, Ito F, van Born S, Huybrechts R, Volckaert F, Billen J (1998) Widespread occurrence of the micro-organism Wolbachia in ants. Proc R Soc Lond B 265:1447–1452

    Article  CAS  Google Scholar 

  • Werren JH (1991) The paternal-sex-chromosome of Nasonia. Am Nat 137:392–402

    Article  Google Scholar 

  • Wheeler WM (1905) The ants of the bahamas, with a list of the known West Indian species. Bo Am Mus Nat Hist 21:79–135

    Google Scholar 

  • Whiting PW (1939) Sex determination and reproductive economy in Habrobracon. Genetics 24:110–111

    Google Scholar 

  • Wilson EO (1988) The biogeography of the West Indian ants (Hymenoptera: Formicidae). In: Liebherr JK (ed) Zoogeography of Caribbean insects. Cornell University Press, New York, pp 214–230

    Google Scholar 

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Acknowledgments

We thank Jon N. Seal and two anonymous referees for critical comments on the manuscript. Jon N. Seal, Jan Oettler, Bartosz Walter, Christiane Wanke, Benjamin Barth and Simon Tragust kindly assisted ant collecting in the field. We acknowledge the following individuals and institutions for facilitating the necessary collection and export permits: Miguel A. García, Departamento de Recursos Naturales y Ambientes, Puerto Rico; Amarilis Polonia, Dirección General de Vida Silvestre y Biodiversidad, Dominican Republic; James Arlington, Ministry of Agriculture, Fisheries and Forestry, Dominica; Ian Gibbs, Ministry of Agriculture and Rural Development, Barbados; Dr Bowen Louison, Ministry of Agriculture, Grenada; Tamica Rahming, Bahamas National Trust; Wilber Sabido, Ministry of Natural Resources and the Environment, and the Belize Audubon Society; Ernest Cowan, Florida Department of Environmental Protection, and the staff at John Pennekamp, Coral Reef State Park and Curry Hammock State Park; Donna Berry at the Nature Conservancy’s Southmost Preserve, and Jimmy Paz at the Texas Audubon Society at the Sabal Palm Grove; Lucia Orantes and Jorge Ivan Restrepo Zamorano Center of Biodiversity, Pan-American School of Agriculture, Honduras. This project is supported by Deutsche Forschungsgemeinschaft (DFG, He 1623/20).

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Correspondence to Katrin Kellner.

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Kellner, K., Heinze, J. Mechanism of facultative parthenogenesis in the ant Platythyrea punctata . Evol Ecol 25, 77–89 (2011). https://doi.org/10.1007/s10682-010-9382-5

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