Elsevier

Animal Behaviour

Volume 135, January 2018, Pages 109-119
Animal Behaviour

Worker thelytoky allows requeening of orphaned colonies but increases susceptibility to reproductive cheating in an ant

https://doi.org/10.1016/j.anbehav.2017.11.013Get rights and content

Highlights

  • Conflicts over worker reproduction are costly in the ant C. cursor.

  • Worker thelytoky allows requeening under quasinatural conditions.

  • Worker thelytoky is associated with low reproductive cheating and social parasitism.

  • Thelytoky probably evolved in the queen caste but not in the worker caste.

In some social insects, workers can produce females asexually through thelytokous parthenogenesis. This allows them to produce replacement queens (i.e. requeening) if the queen has died, but also to compete with the queen to produce females (i.e. reproductive cheating). For the first time, we experimentally tested the role of worker thelytoky under quasinatural conditions in the ant Cataglyphis cursor, where the queen uses both sexual and thelytokous reproduction. We reared pairs of orphaned and queenright colonies in enclosures for almost 3 months, during which they competed for resources. Orphaned colonies lost more workers than queenright colonies over the course of the experiment, presumably because of the costs of reproductive conflicts between workers. Nevertheless, they produced new queens through worker thelytoky and new colonies through colony fission. This is the first unambiguous demonstration that worker thelytoky allows requeening under natural conditions in this species. We further showed that worker thelytoky results in reproductive cheating in the form of a few workers reproducing in the presence of the queen (in queenright colonies) and a few worker lineages producing more new queens than other lineages (in orphaned colonies). In addition, it also results in rare instances of social parasitism, that is, workers entering and reproducing in foreign colonies. These benefits to workers seem too occasional and too low to drive the evolution of thelytoky in this species. We argue that thelytoky probably evolved in the queen caste, where it allows the production of young queens and confers frequent and large benefits by increasing gene transmission, but is also expressed in workers because of genetic correlations between the two castes.

Section snippets

Colony Collection and Experiment

At the end of the hibernation period (8–10 March 2011), 18 colonies were completely excavated in the population of Argelès-sur-Mer near Perpignan (42.5722°N, 3.0437°E). They contained an average of 961.8 workers (range 427–2101) and no brood (Appendix Table A1). Two of these colonies were collected with no queen. Whether the queen died during hibernation or was lost during excavation is unclear. Colonies were then paired by colony size, with each pair comprising one queenright and one queenless

Success of Queenright and Queenless Colonies

At least two nests were found in each enclosure, and they matched the two colonies initially transplanted in the enclosures. The process of colony fission had started at the time of colony collection in five enclosures where more than two nests were recovered (Fig. 1). Newly founded nests contained fewer workers (median 56 workers, quartiles 40–103) and no or few gynes and hence could not be confounded with the two colonies initially transplanted, which were more populous (median 314 workers,

Discussion

In many species of social insects, colonies that are orphaned die. In others, the lost queen is replaced, and the colony carries on, but being orphaned is still a critical situation during which the colony's functioning is disturbed and its growth is poor. In addition, orphaned colonies are predicted to be particularly prone to reproductive conflicts in polyandrous species (Châline et al., 2003, Chéron, Monnin et al., 2011, Hughes and Boomsma, 2008), especially in species where workers can

Data accessibility statement

Genetic analyses reported in this article can be reproduced using the data published in Mendeley (https://doi.org/10.17632/83j7xtw6fm.2).

Acknowledgments

We thank the Laboratoire Arago (Observatoire Océanologique de Banyuls-sur-mer, Université Pierre et Marie Curie) for permitting this study to take place on the experimental grounds of the Mediterranean Garden of Mas de la Serre. We thank David Sillam-Dussès, Fabien Aubrun, Romain Péronnet and Claire Tirard for help in collecting colonies.

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