In this study, we used the black garden ant Lasius niger to investigate the benefits and factors of pleometrosis, the transitory association between founding queens. The monitoring of colonies founded by one or two queens showed that pleometrosis increased and accelerated offspring production. Then, the experimental pairing of L. niger founding queens revealed that in pairs of queens of different fecundity but similar size, the most fecund queen was more likely to survive. Our experiment could not detect a similar effect of size when controlling for fecundity. Finally, we found that queens associated preferentially with less fecund queens.
Our findings of pleometrosis benefiting offspring production are in line with the literature for this, and other ant species3,7,9,10,12,22,23. Interestingly, we only detected these benefits at the colony level, as pleometrosis had either no effect or a negative influence on the per capita offspring production9,12,22. However, colony-level measurements are more relevant in the case of pleometrosis, as the queen that survives the association inherits all the offspring produced during colony foundation. In the field, colonies with a faster, more efficient worker production would have a competitive advantage over neighbouring founding colonies3,4. This is especially true for L. niger, which shows high density of founding colonies that compete for limiting resources and raid the brood of other colonies10. Thus, the competitive advantage provided by pleometrosis likely enhances colony growth and survival.
The increased and faster production of workers in colonies with two queens may stem from a nutritional boost for the larvae. L. niger founding queens do not forage, and produce the first cohort of workers from their own metabolic reserves. Larvae have been observed to cannibalize both viable and non-viable (trophic) eggs24. We found that colonies with two queens produced more eggs, but that this did not translate in them having more larvae. However, more of these larvae became pupae—and ultimately workers. In addition, while the time to produce the first egg and larva did not differ between colonies with one and two queens, the first pupa and worker were produced faster when two queens were present, consistent with a shorter larval stage. We propose that larvae in pleometrotic colonies developed faster and were more likely to reach pupation because they had more eggs that provided nutrients, boosting the development rate of the first workers.
These benefits of pleometrosis are only inherited by the queens that survive, it is thus important to understand the factors that determine queen survival in pleometrotic associations. Although this question has been relatively well studied3,16,17,18,19,20,21, it has remained challenging to disentangle the effects of correlated factors. For example, we found that size, which has been reported to predict queen survival16,19, correlated with fecundity, which would itself be confounded with the parentage of workers in the first cohort produced. To address this issue, we disentangled size and fecundity experimentally, and used foreign workers that developed from pupae collected in field colonies to prevent any potential nepotistic behaviour.
We found that fecundity, but not size, determined queen survival. The finding that, despite being of similar size, more fecund queens are more likely to survive indicates that the outcome of pleometrosis is not the mere consequence of physical dominance. The higher fecundity could reflect a better health condition, which may give the advantage to the more fecund queen in direct fights3,15, or if workers initiate the fights. Natural selection may have favoured workers that skew aggression toward the less fecund queen, both because this queen would be less efficient at building a colony, and because the workers would be more likely to be the offspring of the more fecund queen. The latter would not necessarily involve direct nepotistic behaviours (the workers would not behave according to parentage, but to fecundity), which have remained elusive in social insects in general25,26,27, and in pleometrotic associations in particular16,17,20. Despite regular behavioural observations, we did not observe who initiated aggression in our experiments, and it remains unclear whether the queens and/or the workers are responsible for the onset of fights. Consistently with previous studies16,23, we found that a certain proportion of queen death occurred before worker emergence, suggesting that worker presence is not required for queen execution. Finally, we cannot rule out that the least fecund queens were more likely to die because of a weaker health status, possibly combined with the stress of being associated with another, healthier queen.
Although it has not been directly reported before, our finding that fecundity determines queen survival is consistent with previous reports of weight being associated with queen survival17, more fecund queens being more aggressive28, cuticular hydrocarbon profiles differing between surviving and culled queens21, and between more and less fecund queens28. We could not directly support previous reports of size correlating with survival16,19. This could be because in those studies, size could have been confounded with fecundity, and/or because we lacked the statistical power to detect such effect in our experiment.
Pleometrosis provides clear benefits, but these benefits are only inherited by the surviving queens, and the losing queens pay the great cost of dying without contributing to the next generation. Natural selection should thus favour queens that decide whether or not to join a pleometrotic association based on the relative benefits compared to individual foundation—these may differ across ecological contexts29—and the likelihood of surviving the association. As fecundity appears to determine queen survival in L. niger, queens may have evolved the ability to choose among potential partners according to their fecundity. Our results are consistent with this hypothesis, as queens preferentially associated with partners that would later produce fewer eggs, possibly because they were less fecund, and therefore less healthy and easier to eliminate. This suggests that founding queens may assess the fecundity of potential partners, possibly via their cuticular hydrocarbon profile28. This result further supports our finding that fecundity plays an important role in pleometrotic associations. It is important to note that this difference in egg production could have alternative explanations. First, it could stem from more fecund queens having no interest in forming an association because they are able to start a competitive colony alone. Second, it could be a consequence, rather than a cause, of the outcome of the choice experiment. We cannot rule out that entering an association with another queen and/or leaving this association prematurely at the end of the choice experiment may have been stressful for the chosen queens, and affected their later production of eggs. We could not detect any difference between chosen and not chosen queens in the number of larvae and pupae produced, which are likely influenced by factors other than fecundity (e.g., brood care behaviour). Interestingly, we did not find that queens chose according to size, consistent with our finding that size may not affect which queen survives the pleometrotic association.
Our study informs on the benefits and factors of pleometrosis, and highlights the role of fecundity in the decision to associate with another queen, and in determining which queen survives the association. As such, it contributes to a better understanding of the onset and outcome of pleometrosis, a classic case of cooperation between unrelated animals.
Source: Ecology - nature.com
