The distribution of thelytoky, arrhenotoky and androgenesis among castes in the eusocial Hymenoptera

Review Article

Abstract

Thelytokous parthenogenesis is the production of females from unfertilized eggs. In this review we categorize the known thelytokous eusocial Hymenopterans (mostly ants) by their modes of worker and queen reproduction. The resultant tabulation reveals that: (1) there are no species in which queens are thelytokous and workers are exclusively arrhenotokous (asexual production of males). (2) When workers are capable of thelytoky, there are no examples of species in which queens are strictly thelytokous. (3) Strict queen thelytoky is only present in species with irreversibly sterile workers. (4) Facultative queen thelytoky and sterile workers can lead to the evolution of androgenesis (males are clonal sons of their fathers). These associations are probably best explained by consideration of differing fitness benefits of thelytoky between workers and queens and suggest that some combinations are unlikely to evolve. We therefore predict that they will hold for all eusocial Hymenoptera. No examples of endobacterium-induced thelytoky are known for the eusocial Hymenoptera, whereas endobacterium-induced thelytoky is widespread in the solitary Hymenoptera. We argue that this is because species in which both queens and workers are thelytokous that are unlikely to persist over evolutionary time. Further, eusocial species have single-locus sex determination, which is not compatible with endobacterium-induced feminization that is typically based on genome duplication. Only two thelytokous eusocial bees are known, and their modes of reproduction are consistent with the associations seen in ants. Thus far, no thelytokous eusocial wasps have been identified.

Keywords

Thelytoky Parthenogenesis Kin selection Eusocial Queen-worker conflict 

Notes

Acknowledgements

We thank members of the Behaviour and Genetics of Social Insects lab for comments on the manuscript, many anonymous (and not so anonymous, thanks Serge!) reviewers who have commented on previous versions, and the Australian Research Council for support (project DP 150101985).

Glossary

Androgenesis

Clonal production of a male with no maternal genomic contribution to embryo as occurs in some ants.

Arrhenotoky

Virgin birth of a male from a female (e.g., most Hymenopteran males).

Automixis

Following a meiotic cell division, two of the four haploid cells fuse to restore diploidy. Necessary for thelytokous parthenogenesis seen in eusocial Hymenoptera.

Central fusion

Following a meiotic cell division there are two pairs of cells each pair derived from the division of a different cell of meiosis I. When the two central cells fuse this is central fusion. Central fusion has the effect of restoring most of the genome and heterozygosity of the mother because the two central nuclei are derived from different parental cells. Compare with terminal fusion.

Centromeric

Near the centromere of a chromosome. Recombination is reduced near the centromere.

Hybridogen

Offspring of the mating of two species or lineages with elimination of the paternal or maternal genome. Occurs in some Cataglyphis where workers are hybrids, but queens and males are produced asexually by the respective lineages.

Parthenogenesis

Virgin birth.

Terminal fusion

Following a meiotic cell division there are two pairs of cells each pair derived from the division of a single cell of meiosis I. When two terminal cells fuse this is terminal fusion. Terminal fusion has the effect of losing most of the heterozygosity of the mother because the terminal nuclei are derived from the same parent cell. Compare with central fusion.

Telomeric

Towards the end of a chromosome.

Thelytoky

Virgin birth of a female from a female.

References

  1. Amor F, Ortega P, Boulay R, Cerdá X (2017) Frequent colony orphaning triggers the production of replacement queens via worker thelytoky in a desert-dwelling ant. Insectes Soc 64:373–378.  https://doi.org/10.1007/s00040-017-0556-9 CrossRefGoogle Scholar
  2. Anderson RH (1968) The effect of queen loss on colonies of Apis mellifera capensis. S Afr J Agric Sci 11:368–388Google Scholar
  3. Aron S, Darras H, Eyer P-A, Leniaud L, Pearcy M (2013) Structure génétique des sociétés et systèmes d’accouplement chez la fourmi Cataglyphis viatica (Fabricius 1787). Bull Inst Sci Rabat Sec Sci Vie 35:103–109Google Scholar
  4. Aron S, Mardulyn P, Leniaud L (2016) Evolution of reproductive traits in Cataglyphis desert ants: mating frequency, queen number, and thelytoky. Behav Ecol Sociobiol 70:1367–1379.  https://doi.org/10.1007/s00265-016-2144-9 CrossRefGoogle Scholar
  5. Aumer D, Allsopp MH, Lattorff HMG, Moritz RFA, Jarosch-Perlow A (2017) Thelytoky in Cape honeybees (Apis mellifera capensis) is controlled by a single recessive locus. Apidologie 48:401–410.  https://doi.org/10.1007/s13592-016-0484-0 CrossRefGoogle Scholar
  6. Beekman M, Allsopp MH, Jordan LA, Lim J, Oldroyd BP (2009) A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis. Mol Ecol 18:2722–2727.  https://doi.org/10.1111/j.1365-294X.2009.04224.x CrossRefPubMedGoogle Scholar
  7. Beekman M, Allsopp MH, Lim J, Goudie F, Oldroyd BP (2011) Asexually produced Cape honeybee queens (Apis mellifera capensis) reproduce sexually. J Hered 102:562–566.  https://doi.org/10.1093/jhered/esr075 CrossRefPubMedGoogle Scholar
  8. Beekman M, Oldroyd BP (2008) When workers disunite: intraspecific parasitism in eusocial bees. Annu Rev Entomol 53:19–37.  https://doi.org/10.1146/annurev.ento.53.103106.093515 CrossRefPubMedGoogle Scholar
  9. Beukeboom LW, Pijnacker LP (2000) Automictic parthenogenesis in the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) revisited. Genome 43:939–944.  https://doi.org/10.1139/g00–061CrossRefPubMedGoogle Scholar
  10. Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419–429.  https://doi.org/10.1016/S0092-8674(03)00606-8 CrossRefPubMedGoogle Scholar
  11. Bourke AFG (2011) Principles of social evolution. Oxford University Press, New YorkCrossRefGoogle Scholar
  12. Cagniant H (1979) La parthénogenèse thélytoque et arrhénotoque chez la fourmi Cataglyphis cursor Fonsc. (Hym., Form.). Cycle biologique en élevage des colonies avec reine et des colonies sans reine. Insectes Soc 26:51–60.  https://doi.org/10.1007/BF02283912 CrossRefGoogle Scholar
  13. Cagniant H (1980) La parthénogenèse thélytoque et arrhénotoque des ouvrières de la fourmi Cataglyphis cursor Fonscolombe. Insectes Soc 27:157–174.  https://doi.org/10.1007/BF02229251 CrossRefGoogle Scholar
  14. Cagniant H (1982) La parthénogenèse thélytoque et arrhénotoque chez la fourmi Cataglyphis cursor Fonscolombe (Hymenoptera, Formicidae). Étude des œufs ponduc par les reines et les ouvrières: morphologie, devenir, influence sur le déterminisme de la caste reine. Insectes Soc 29:175–188.  https://doi.org/10.1007/BF02229251 CrossRefGoogle Scholar
  15. Cagniant H (1983) La parthénogenèse thélytoque et arrhénotoque des ouvières de la fourmi Cataglyphis cursor Fonscolombe (Hymenoptères Formicidae). Étude biométrique des ouvrières et de leurs potentialités reproductrices. Insectes Soc 30:241–254.  https://doi.org/10.1007/BF02223982 CrossRefGoogle Scholar
  16. Chapman NC, Beekman M, Allsopp MH, Rinderer TE, Lim J, Oxley PR, Oldroyd BP (2015) Inheritance of thelytoky in the honey bee Apis mellifera capensis. Heredity 114:584–592.  https://doi.org/10.1038/hdy.2014.127 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Clemencet J, Rome Q, Federici P, Doums C (2008) Aggressions and size-related fecundity of queenless workers in the ant Cataglyphis cursor. Naturwissenschaften 95:133–139.  https://doi.org/10.1007/s00114-007-0304-5 CrossRefPubMedGoogle Scholar
  18. Cole-Clark MP, Barton DA, Allsopp MH, Beekman M, Gloag RS, Wossler TC, Ronai I, Smith N, Reid RJ, Oldroyd BP (2017) Cytogenetic basis of thelytoky in Apis mellifera capensis. Apidologie 48(5):623–634.  https://doi.org/10.1007/s13592-017-0505-7 623–634.CrossRefGoogle Scholar
  19. Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286.  https://doi.org/10.1016/0169-5347(95)90011-X CrossRefPubMedGoogle Scholar
  20. Cordaux R, Bouchon D, Greve P (2011) The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27:332–341.  https://doi.org/10.1016/j.tig.2011.05.002 CrossRefPubMedGoogle Scholar
  21. Crawley WC (1912) Parthenogenesis in worker ants, with special reference to two colonies of Lasius niger, Linn. Trans R Entomol Soc Lond 59:657–663CrossRefGoogle Scholar
  22. Crewe R, Allsopp M (1994) Sex and the single queen: recent experiments with capensis and scutellata queens. S Afr Bee J 66:58–62Google Scholar
  23. Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  24. Dartigues D, Lenoir A (1990) La ponte des ouvrières Cataglyphis bicolor F. (Hymenoptera: Formicidae): mise en évidence d’une parthénogénèse thélytoque. Ann Soc Entomol Fr 26:121–123Google Scholar
  25. Darwin C (1859) The origin of species. Murray, LondonGoogle Scholar
  26. Dietemann V, Peeters C (2000) Queen influence on the shift from trophic to reproductive eggs laid by workers of the ponerine ant Pachycondyla apicalis. Insectes Soc 47:223–228.  https://doi.org/10.1007/PL00001707 CrossRefGoogle Scholar
  27. Dobata S, Sasaki T, Mori H, Hasegawa E, Shimada M, Tsuji K (2009) Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus. Proc R Soc B 276:567–574.  https://doi.org/10.1098/rspb.2008.1215 CrossRefPubMedGoogle Scholar
  28. Doums C, Cronin AL, Ruel C, Fédérici P, Haussy C, Tirard C, Monnin T (2013) Facultative use of parthenogenesis for queen production in the polyandrous ant Cataglyphis cursor. J Evol Biol 26:1431–1444.  https://doi.org/10.1111/jeb.12142 CrossRefPubMedGoogle Scholar
  29. Ebert D, Hamilton WD (1996) Sex against virulence: the coevolution of parasitic diseases. Trends Ecol Evol 11:79–82CrossRefPubMedGoogle Scholar
  30. Engelstädter J (2008) Constraints on the evolution of asexual reproduction. BioEssays 30:1138–1150.  https://doi.org/10.1002/bies.20833 CrossRefPubMedGoogle Scholar
  31. Eyer PA, Leniaud L, Darras H, Aron S (2013) Hybridogenesis through thelytokous parthenogenesis in two Cataglyphis desert ants. Mol Ecol 22:947–955.  https://doi.org/10.1111/mec.12141 CrossRefPubMedGoogle Scholar
  32. Foucaud J, Estoup A, Loiseau A, Rey O, Orivel J (2010) Thelytokous parthenogenesis, male clonality and genetic caste determination in the little fire ant: new evidence and insights from the lab. Heredity 105:205–212.  https://doi.org/10.1038/hdy.2009.169 doiCrossRefPubMedGoogle Scholar
  33. Foucaud J, Fournier D, Orivel J, Delabie JHC, Loiseau A, Le Breton J, Kergoat GJ, Estoup A (2007) Sex and clonality in the little fire ant. Mol Biol Evol 24:2465–2473.  https://doi.org/10.1093/molbev/msm180 CrossRefPubMedGoogle Scholar
  34. Fournier D, Aron S (2009) Evolution: No-male’s land for an Amazonian ant. Curr Biol 19:R739.  https://doi.org/10.1016/j.cub.2009.07.021 CrossRefGoogle Scholar
  35. Fournier D, Estoup A, Orivel RM, Foucaud J, Jourdan H, Le Breton J, Keller L (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234.  https://doi.org/10.1038/nature03705 CrossRefPubMedGoogle Scholar
  36. Frumhoff PC, Ward PS (1992) Individual-level selection, colony-level selection, and the association between polygyny and worker monomorphism in ants. Am Nat 139:559–590.  https://doi.org/10.1086/285344 CrossRefGoogle Scholar
  37. Gloag R, Ding G, Christe JR, Buchmann G, Beekman M, Oldroyd BP (2016) An invasive social insect overcomes genetic load at the sex locus. Nature Ecol Evol 1:11.  https://doi.org/10.1038/s41559-016-0011 CrossRefGoogle Scholar
  38. Gößwald K (1962) Zur Kastendetermination der Ameisen unter besonderer Berücksichtigung trophogener Faktoren. Symp Genet Biol Ital 10:106–168Google Scholar
  39. Gotoh A, Billen J, Tsuji K, Sasaki T, Ito F (2012) Histological study of the spermatheca in three thelytokous parthenogenetic ant species, Pristomyrmex punctatus, Pyramica membranifera and Monomorium triviale (Hymenoptera: Formicidae). Acta Zool 93:200–207.  https://doi.org/10.1111/j.1463-6395.2010.00498.x CrossRefGoogle Scholar
  40. Goudie F, Allsopp MH, Beekman M, Oxley PR, Lim J, Oldroyd BP (2012) Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis mellifera). Evolution 66:1897–1906.  https://doi.org/10.1111/j.1558-5646.2011.01543.x CrossRefPubMedGoogle Scholar
  41. Goudie F, Allsopp MH, Oldroyd BP (2014) Selection on overdominant genes maintains heterozygosity along multiple chromosomes in a clonal lineage of honey bee. Evolution 68:125–136.  https://doi.org/10.1111/evo.12232 CrossRefPubMedGoogle Scholar
  42. Goudie F, Allsopp MH, Solignac M, Beekman M, Oldroyd BP (2015) The frequency of arrhenotoky in the normally thelytokous Apis mellifera capensis worker and the clone reproductive parasite. Insectes Soc 62:352–333.  https://doi.org/10.1007/s00040-015-0401-y CrossRefGoogle Scholar
  43. Goudie F, Oldroyd BP (2014) Thelytoky in the honey bee. Apidologie 45:306–326.  https://doi.org/10.1007/s13592-013-0261-2 CrossRefGoogle Scholar
  44. Grangier J, Avril A, Lester PJ (2013) Male production by workers in the polygynous ant Prolasius advenus. Insectes Soc 60:303.  https://doi.org/10.1007/s00040-013-0294-6 CrossRefGoogle Scholar
  45. Grasso DA, Wenseleers T, Mori A, Le Moli F, Billen J (2000) Thelytokous worker reproduction and lack of Wolbachia infection in the harvesting ant Messor capitatus. Ethol Ecol Evol 12:309–314CrossRefGoogle Scholar
  46. Greeff JM (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Philos Trans R Soc Lond B 351:617–625.  https://doi.org/10.1098/rstb.1996.0060 CrossRefGoogle Scholar
  47. Gruber MAM, Ritchie PA, Lester PJ, Hoffmann BD (2013) The conundrum of the yellow crazy ant (Anoplolepis gracilipes) reproductive mode: no evidence for dependent lineage genetic caste determination. Insectes Soc 60:135–145.  https://doi.org/10.1007/s00040-012-0277-z CrossRefGoogle Scholar
  48. Hagimori T, Abe Y, Date S, Miura K (2006) The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Curr Microbiol 52:97–101.  https://doi.org/10.1007/s00284-005-0092-0 CrossRefPubMedGoogle Scholar
  49. Holmes MJ, Tan K, Wang Z, Oldroyd BP, Beekman M (2014) Genetic reincarnation of workers as queens in the Eastern honeybee Apis cerana. Heredity 114:65–68.  https://doi.org/10.1038/hdy.2014.70 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Hoy MA, Jeyaprakash A, Alverez JM, Allsopp M (2003) Wolbachia is present in Apis mellifera capensis, A.m. scutellata, and their hybrid in South Africa. Apidologie 34:53–60.  https://doi.org/10.1051/apido:2002048 CrossRefGoogle Scholar
  51. Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260CrossRefPubMedGoogle Scholar
  52. Huigens ME, Stouthamer R (2003) Parthenogenesis associated with Wolbachia. In: Bourtzis K, Miller TA (eds) Insect symbiosis. CRC Press, Boca Raton, pp 247–266Google Scholar
  53. Ito F, Touyama Y, Gotoh A, Kitahiro S, Billen J (2010) Thelytokous parthenogenesis by queens in the dacetine ant Pyramica membranifera (Hymenoptera: Formicidae). Naturwissenschaften 97:725–728.  https://doi.org/10.1007/s00114-010-0688-5 CrossRefPubMedGoogle Scholar
  54. Itow T, Kobayashi K, Kubota M, Ogata K, Imai HT, Crozier RH (1984) The reproductive cycle of the queenless ant Pristomyrmex pungens. Insectes Soc 31:87–102CrossRefGoogle Scholar
  55. Jones J, Myerscough M, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404.  https://doi.org/10.1126/science.1096340 CrossRefPubMedGoogle Scholar
  56. Kellner K, Heinze J (2011) Mechanism of facultative parthenogenesis in the ant Platythyrea punctata. Evol Ecol 25:77–89.  https://doi.org/10.1007/s10682-010-9382-5 CrossRefGoogle Scholar
  57. Khila A, Abouheif E (2010) Evaluating the role of reproductive constraints in ant social evolution. Philos Trans R Soc B 365:617–630.  https://doi.org/10.1098/rstb.2009.0257 CrossRefGoogle Scholar
  58. Kobayashi K, Hasegawa E, Ohkawara K (2008) Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler). Entomol Sci 11:167–172.  https://doi.org/10.1111/j.1479-8298.2008.00272.x CrossRefGoogle Scholar
  59. Kronauer DJC, Pierce NE, Keller L (2012) Asexual reproduction in introduced and native populations of the ant Cerapachys biroi. Mol Ecol 21:5221–5235.  https://doi.org/10.1111/mec.12041 CrossRefPubMedGoogle Scholar
  60. Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292–295.  https://doi.org/10.1098/rsbl.2007.0083 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Leniaud L, Darras H, Boulay R, Aron S (2012) Social hybridogenesis in the clonal ant Cataglyphis hispanica. Curr Biol 22:1186–1193.  https://doi.org/10.1016/j.cub.2012.04.060 CrossRefGoogle Scholar
  62. Leniaud L, Hefetz A, Grumiau L, Aron S (2011) Multiple mating and supercoloniality in Cataglyphis desert ants. Biol J Linn Soc 104:866–876.  https://doi.org/10.1111/j.1095-8312.2011.01772.x CrossRefGoogle Scholar
  63. Masuko K (2013) Thelytokous parthenogenesis in the ant Strumigenys hexamera (Hymenoptera: Formicidae). Ann Entomol Soc Am 106:479–484.  https://doi.org/10.1603/AN12144 CrossRefGoogle Scholar
  64. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364.  https://doi.org/10.1126/science.1143046 CrossRefPubMedGoogle Scholar
  65. Normark BB (2003) The evolution of alternative genetic systems in insects. Annu Rev Entomol 48:397–423.  https://doi.org/10.1146/annurev.ento.48.091801.112703 CrossRefPubMedGoogle Scholar
  66. Ohkawara K, Makayama 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.  https://doi.org/10.1098/rsbl.2006.0491 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Okita I, Tsuchida K (2016) Clonal reproduction with androgenesis and somatic recombination: the case of the ant Cardiocondyla kagutsuchi. Sci Nat 103.  https://doi.org/10.1007/s00114-016-1349-0
  68. 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.  https://doi.org/10.1534/genetics.108.090415 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Oldroyd BP, Allsopp MH, Lim J, Beekman M (2011) A thelytokous lineage of socially parasitic honey bees has retained heterozygosity despite at least 10 years of inbreeding. Evolution 65:860–868.  https://doi.org/10.1111/j.1558-5646.2010.01164.x CrossRefPubMedGoogle Scholar
  70. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413.  https://doi.org/10.1016/j.tree.2007.06.001 CrossRefPubMedGoogle Scholar
  71. Pearcy M, Aron S, Doums C, Keller L (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306:1780–1783.  https://doi.org/10.1126/science.1105453 CrossRefPubMedGoogle Scholar
  72. Pearcy M, Goodisman MAD, Keller L (2011) Sib mating without inbreeding in the longhorn crazy ant. Proc R Soc Lond B 278:2677–2681.  https://doi.org/10.1098/rspb.2010.2562 CrossRefGoogle Scholar
  73. Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382.  https://doi.org/10.1038/sj.hdy.6800813 CrossRefPubMedGoogle Scholar
  74. Rabeling C, Gonzales O, Schultz TR, Bacci M, Garcia MVB, Verhaagh M, Ishak HD, Meuller UG (2011) Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungus-growing ant. Proc Natl Acad Sci USA 108:12366–12371.  https://doi.org/10.1073/pnas.1105467108 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rabeling C, Kronauer DJC (2013) Thelytokous parthenogenesis in eusocial Hymenoptera. Annu Rev Entomol 58:273–292.  https://doi.org/10.1146/annurev-ento-120811-153710 CrossRefPubMedGoogle Scholar
  76. Rabeling C, Lino-Neto J, Cappellari SC, Dos-Santos IA, Mueller UG, Bacci M Jr (2009) Thelytokous parthenogenesis in the fungus-gardening ant Mycocepurus smithii (Hymenoptera: Formicidae). PLoS One 4:e6781.  https://doi.org/10.1371/journal.pone.0006781 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Ravary F, Jaisson P (2002) The reproductive cycle of thelytokous colonies of Cerapachys biroi Forel (Formicidae, Cerapachyinae). Insectes Soc 49:114–119.  https://doi.org/10.1007/s00040-002-8288-9 CrossRefGoogle Scholar
  78. Reichenbach H (1902) Über Parthenogenese bei Ameisen und anderen Beobachtungen an Ameisenkolonien in künstlichen Nestern. Biol Centralblatt 22:491–465Google Scholar
  79. Rey O, Facon B, Foucaud J, Loiseau A, Estoup A (2013) Androgenesis is a maternal trait in the invasive ant Wasmannia auropunctata. Proc R Soc Lond B 280:2013118170.  https://doi.org/10.1098/rspb.2013.1181 CrossRefGoogle Scholar
  80. Ronai I, Vergoz V, Oldroyd BP (2016) The mechanistic, genetic, and evolutionary basis of worker sterility in the social Hymenoptera. Adv Stud Behav 48:251–317.  https://doi.org/10.1016/bs.asb.2016.03.002 CrossRefGoogle Scholar
  81. Schilder K, Heinze J, Gross R, Holldobler B, Smith F (1999) Microsatellites reveal clonal structure of populations of the thelytokous ant Platythyrea punctata (Hymenoptera; Formicidae). Mol Ecol 8:1497–1507.  https://doi.org/10.1046/j.1365-294x.1999.00727.x CrossRefPubMedGoogle Scholar
  82. Schneider MV, Driessen G, Beukeboom LW, Boll R, van Eunen K, Selzner A, Talsma J, Lapchin L (2003) Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera). Heredity 90:260–267.  https://doi.org/10.1038/sj.hdy.6800245 CrossRefPubMedGoogle Scholar
  83. Schwander T, Oldroyd BP (2016) Androgenesis: where males hijack eggs to clone themselves. Philos Trans R Soc B 371:20150534.  https://doi.org/10.1098/rstb.2015.0534 CrossRefGoogle Scholar
  84. Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc Lond B 274:67–72.  https://doi.org/10.1098/rspb.2006.3702 CrossRefGoogle Scholar
  85. Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens and polyandry in social Hymenoptera. Am Nat 131:602–610.  https://doi.org/10.1086/284809 CrossRefGoogle Scholar
  86. Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca RatonGoogle Scholar
  87. Timmermans I, Grumiau L, Hefetz A, Aron S (2010) Mating system and population structure in the desert ant Cataglyphis livida. Insectes Soc 57:39–46.  https://doi.org/10.1007/s00040-009-0048-7 CrossRefGoogle Scholar
  88. Timmermans I, Hefetz A, Fournier D, Aron S (2008) Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa. Heredity 101:490–498.  https://doi.org/10.1038/hdy.2008.72 CrossRefPubMedGoogle Scholar
  89. Tschinkel WR (2006) The fire ants. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  90. Tsuji K, Yamauchi K (1995) Production of females by parthenogenesis in the ant, Cerapachys biroi. Insectes Soc 42:333–336.  https://doi.org/10.1007/BF01240430 CrossRefGoogle Scholar
  91. van der Kooi CJ, Schwander T (2014) Evolution of asexuality via different mechanisms in grass thrips (Thysanoptera: Aptinothrips). Evolution 68:1883–1893.  https://doi.org/10.1111/evo.12402 CrossRefPubMedGoogle Scholar
  92. Verma S, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the Cape honeybee (Apis mellifera capensis Escholtz). Apidologie 14:41–57CrossRefGoogle Scholar
  93. Wenseleers T, Billen J (2000) No evidence for Wolbachia-induced parthenogenesis in the social Hymenoptera. J Evol Biol 13:277–280.  https://doi.org/10.1046/j.1420-9101.2000.00168.x CrossRefGoogle Scholar
  94. Wenseleers T, Hart AG, Ratnieks FLW (2004) When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. Am Nat 164:E154–E167.  https://doi.org/10.1086/425223 CrossRefGoogle Scholar
  95. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751.  https://doi.org/10.1038/nrmicro1969 CrossRefPubMedGoogle Scholar
  96. Zchori-Fein E, Gottlieb Y, Kelly SE, Brown JK, Wilson JM, Karr TL, Hunter MS (2001) A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc Natl Acad Sci USA 98:12555–12560.  https://doi.org/10.1073/pnas.221467498 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2017

Authors and Affiliations

  1. 1.Behaviour and Genetics of Social Insects Laboratory, Macleay Building A12University of SydneySydneyAustralia

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