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

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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.

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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).

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Correspondence to Benjamin P. Oldroyd.

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.

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Goudie, F., Oldroyd, B.P. The distribution of thelytoky, arrhenotoky and androgenesis among castes in the eusocial Hymenoptera. Insect. Soc. 65, 5–16 (2018). https://doi.org/10.1007/s00040-017-0597-0

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  • DOI: https://doi.org/10.1007/s00040-017-0597-0

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