Asexual Queen Succession in Termites

Abstract

Termite species from phylogenetically distant lineages were shown to combine both sexual and parthenogenetic reproductions, in a breeding system dubbed as ‘asexual queen succession’. Queens of these species use sexual reproduction for the production of the workforce and dispersers, and thelytokous parthenogenesis for the production of nondispersing queens. These new queens, often produced in large numbers, will replace their mother upon her death and mate with the founding king. Replacement by these parthenogens maintains the colony's genetic diversity and enhances its growth rate, lifespan and reproductive potential. This breeding system also allows the efficient purging of recessive deleterious mutations from the genomes and contributes to shape the population sex ratio of these species. This conditional parthenogenesis evolved from a diverse cytological background, and in phylogenetically distant species with contrasted lifestyles, thereby highlighting the inherent evolutionary advantages of this strategy.

Key Concepts

  • The historical view of a lifelong monogamy between a primary queen and king in termites now appears obsolete.
  • Termite queens of some species combine the advantages of sexual and asexual reproductions in a breeding system called asexual queen succession (AQS).
  • AQS shapes the genomes of these species by the elimination of recessive deleterious mutations through parthenogenetically produced new queens.
  • AQS, along with the species' ecology and lifestyle, influences their population sex ratio.
  • Variations in the modalities of AQS indicate that its benefits are used in a species‐specific manner.

Keywords: eusocial insects; Isoptera; parthenogenesis; reproduction; selective purge; sex ratio; sexual reproduction; thelytoky

Figure 1. Photographs of the humivorous Syntermitinae Silvestritermes minutus. (a) Primary colony headed by a primary king (PK) and a primary queen (PQ). (b) Secondary colony headed by the primary king and numerous parthenogenetically produced neotenic queens. Two generations of neotenic queens can be observed, younger ones with brown tergites and creamy white intersegmental membranes (NQ1) and older ones more ochraceous overall, with lighter tergites and darker intersegmental membranes (NQ2). Soldiers (S) and workers (W) are produced sexually. Scale bars, 2 mm. (a,b) Yves Roisin.
Figure 2. Simplified view of the consequences of reproductives' replacements and modes of reproduction (p, parthenogenesis; s, sexual reproduction) on the genetic structure of the colony and the population through the asymmetric genetic contribution of the primary queen (in orange) and king (in blue) to the next generation of colonies (based on data from the Termitinae Cavitermes tuberosus). Workers, soldiers and (most) alates are produced sexually in all types of colonies. (a) In a strict asexual queen succession (AQS), the primary queen is replaced by parthenogenetically produced neotenic daughters, and no change in relative genetic contribution of primaries to the offspring occurs. The later king replacement induces an asymmetry of gene transmission among the primaries. If king replacement is frequent in the population, females have a higher reproductive value (transmit more genes) than males, and a female‐biased sex ratio is expected in dispersers (future primaries). (b) The queen can also be replaced by sexually produced daughters, which leads to father–daughter inbreeding and more king's genes to be transmitted.
Figure 3. Overview of the cytological mechanisms of ploidy restoration underlying automictic parthenogenesis in termites, considering recombination during meiosis. In the case of gamete duplication, either the haploid ootide divides and recombines or duplicated chromosomes remain in the original cell. In terminal fusion, the ootides resulting from the same secondary oocyte re‐unite. In central fusion, the two central polar nuclei produced from the two secondary oocytes fuse. Recombination at a given locus depends on the distance from the centromere, and the rate of transition to homozygosity (r) varies between modes: gamete duplication results in full homozygosity, terminal fusion in homozygosity except for recombined loci, central fusion in homozygosity for recombined loci only.
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Further Reading

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Hellemans, Simon, and Roisin, Yves(Aug 2020) Asexual Queen Succession in Termites. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029115]