Comparative Analysis of Worker Reproduction and Policing in Eusocial Hymenoptera Supports Relatedness Theory

Abstract

In many bees, wasps, and ants, workers police each other in order to prevent individual workers from selfishly producing their own male offspring. Although several factors can selectively favor worker policing, genetic relatedness is considered to be of special importance. In particular, kin selection theory predicts that worker policing should be more common in species where workers are more related to the queen's sons than to other workers' sons. Here we provide strong novel support for this theory based on a comparative analysis of policing and male parentage in 109 species of ants, bees, and wasps. First, an analysis of behavioral data confirms that worker policing occurs more frequently in species where workers are more related to the queen's sons than to other workers' sons. Second, an analysis of male parentage shows that a significantly higher percentage of the males are workers' sons in species where the workers are more related to other workers' sons. Both conclusions also hold if data are analyzed using phylogenetically independent contrasts. Although our analysis provides strong overall support for the theory that relatedness affects kin conflict over male parentage, there is also significant residual variation. Several factors that may explain this variation are discussed.Keywords: worker policing, queen policing, worker reproduction, social Hymenoptera, inclusive fitness, kin selection.A major challenge in evolutionary biology is to explain how social groups can reduce or prevent costly conflicts

Altruism in insect societies and beyond: voluntary or enforced?

“…The killing of worker-laid eggs by the queen (queen policing) is also widespread and is particularly common in species with small colonies [5,18]. If policing does coerce altruism by reducing the opportunity for workers to reproduce, we predict that fewer workers should lay eggs in species with more effective egg policing [7,13].…”

“…Evidence for enforced altruism: egg-laying by workers Although worker policing was first discovered in the honeybee [6], it has since been found in several other ant, bee and wasp species [5,18]. The killing of worker-laid eggs by the queen (queen policing) is also widespread and is particularly common in species with small colonies [5,18].…”

“…Enforced cooperation in insect and vertebrate societies and interspecific mutualisms. (a) Worker policing prevents workers from reproducing in the honeybee Apis mellifera [6]; (b) queen policing (inset) prevents most workers from reproducing successfully in the bumblebee Bombus terrestris [18]; (c) a worker with active ovaries is aggressed in the queenless ant Harpegnathos saltator [19]; (d) in the honeybee, differential feeding forces most larvae to develop as workers; only larvae reared in royal cells (arrow) can develop as queens [1,7]; (e) subordinate workers from the allodapine bee Exoneura bicolor are evicted from the nest when they have been in contact with a foreign male [39]; (f) a worker that attempted to overthrow the breeder female is punished in the queenless ant Dinoponera quadriceps [40]; (g) in the cooperatively breeding cichlid Neolamprologus pulcher, subordinates that do not help look after the eggs and fry are evicted [57]; (h) rhesus monkeys (Macaca mulatta) who do not share food are punished [58]; (i) in meerkats (Suricata suricata) dominant females prevent successful breeding by subordinates [62]; (j) soybean plants (Glycine max) sanction root nodule bacteria that do not fix nitrogen, as shown by this split root experiment [55]. …”

Punish or perish? Retaliation and collaboration among humans

“…Economists use experimental games to study the effects of positive and negative incentives (i.e. reward and punishment) on our propensity to collaborate [6,7]; anthropologists visit small-scale societies to measure the culture-dependence and universality of norms that enforce cooperation [8]; psychologists study the often sub-conscious cues eliciting emotions that lead to helping behaviour or moralistic aggression [9][10][11]; neurologists use magnetic resonance techniques to correlate social dilemmas with brain activities [12,13]; game theorists modify their utility functions to take account of non-monetary concerns [14,15]; biologists look for signs of policing and sanctions in bees or bacteria [16,17]; and political scientists attempt to improve governance of institutions promoting collective actions [18,19]. Trans-disciplinary dialogues are in full swing, although communication sometimes needs improving [20].…”

“…Punishment is not the only way to enforce cooperation; harassing those having access to a resource [67], chasing shirkers [68] or sabotaging the attempts of cheaters [16], are different examples, and can also be found in other animals, such as mammals, fishes or insects. But humans, with their cognitive capacities for individual recognition, temporal discounting, memory, empathy and language, are uniquely gifted to develop the proximal mechanisms needed for reciprocation and in particular for punishment.…”