The distribution of thelytoky, arrhenotoky and androgenesis among castes in the eusocial Hymenoptera
- 267 Downloads
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.
KeywordsThelytoky Parthenogenesis Kin selection Eusocial Queen-worker conflict
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).
Clonal production of a male with no maternal genomic contribution to embryo as occurs in some ants.
Virgin birth of a male from a female (e.g., most Hymenopteran males).
Following a meiotic cell division, two of the four haploid cells fuse to restore diploidy. Necessary for thelytokous parthenogenesis seen in eusocial Hymenoptera.
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.
Near the centromere of a chromosome. Recombination is reduced near the centromere.
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.
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.
Towards the end of a chromosome.
Virgin birth of a female from a female.
- Anderson RH (1968) The effect of queen loss on colonies of Apis mellifera capensis. S Afr J Agric Sci 11:368–388Google Scholar
- 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
- 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
- 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
- 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
- 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
- Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
- 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
- Darwin C (1859) The origin of species. Murray, LondonGoogle Scholar
- Gößwald K (1962) Zur Kastendetermination der Ameisen unter besonderer Berücksichtigung trophogener Faktoren. Symp Genet Biol Ital 10:106–168Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Reichenbach H (1902) Über Parthenogenese bei Ameisen und anderen Beobachtungen an Ameisenkolonien in künstlichen Nestern. Biol Centralblatt 22:491–465Google Scholar
- Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca RatonGoogle Scholar
- Tschinkel WR (2006) The fire ants. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
- 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