Sex ratio variations among years and breeding systems in a facultatively parthenogenetic termite

Abstract

Some species of termites evolved an outstanding reproductive strategy called asexual queen succession (AQS), in which the primary queen is replaced by multiple parthenogenetically produced daughters (neotenics) that mate with the primary king. When the primary king is eventually replaced, this time by sexually produced neotenic king(s), sex-asymmetric inbreeding occurs and the queen’s genome is more transmitted than that of the king, thereby increasing the reproductive value of female dispersers, and female-biased population sex ratio is expected. Yet, the life cycle, the breeding system dynamics and AQS modalities differ between AQS species, thereby modifying the relative genetic contribution of primary reproductives in the colony and thus also the equilibrium sex ratio. We estimated colonial and population sex ratio over two consecutive dispersal periods in a French Guiana population of Cavitermes tuberosus (Termitinae) in which the founding queen may be replaced only after colony maturity, some neotenic females may be sexually produced, and some female dispersers arise through parthenogenesis. Colonial sex ratio varied among colonies: primary-headed nests with higher within-nest relatedness produced more females than neotenic-headed nests with lower relatedness among individuals. Over the two dispersal periods, the population investment sex ratio fluctuated around 1:1, thereby confirming that AQS breeding system is not necessarily linked with female-biased sex ratio. The balanced alate sex ratio, combined with the occurrence of sexually produced neotenic queens, is possibly the outcome of a queen-king conflict between the primary reproductives.

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Acknowledgements

We are grateful to Philippe Cerdan, Régis Vigouroux, and the staff of the Laboratoire Environnement HYDRECO of Petit Saut (EDF-CNEH) for logistic support during the field work.

Funding

This work was supported by a PhD fellowship (SH) and grants from the Belgian National Fund for Scientific Research F.R.S.-FNRS (DF and YR: FRFC grant nos. 2.4594.12; DF: J.0110.17), the Research Mobility Project between the Belgian National Fund for Scientific Research FRS-FNRS and the Czech Academy of Sciences (RH and YR: FNRS-17-02) and the project RVO 61388963 (RH, IOCB, Prague).

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Contributions

SH, DF and YR designed the study. SH, RH and YR collected the material. SH performed the molecular laboratory work and genetic analyses. SH, DF and YR carried out the statistical analyses. All authors contributed significantly to the manuscript and approved the final version.

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Correspondence to S. Hellemans.

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Data Archiving

The full dataset of genotypes used is available in the Dryad Data Repository (https://doi.org/10.5061/dryad.01c53v5).

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We dedicate this work to the memory of Philippe Cerdan (1959–2018), co-director of HYDRECO laboratory of Petit Saut in French Guiana.

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Hellemans, S., Fournier, D., Hanus, R. et al. Sex ratio variations among years and breeding systems in a facultatively parthenogenetic termite. Insect. Soc. 66, 129–138 (2019). https://doi.org/10.1007/s00040-018-0667-y

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Keywords

  • Isoptera
  • Parthenogenesis
  • Asexual queen succession
  • Sex ratio
  • Conflict