Punishers Benefit From Third-Party Punishment in Fish

Abstract

H uman studies show that uninvolved bystanders often pay to punish defectors (1, 2). Such behavior has typically been interpreted in terms of group-level benefits (3) despite theoretical predictions that third-party punishment can yield individual benefits to the punisher (4). Here, we show that male cleaner fish, Labroides dimidiatus, punish their female partners if females cheat while inspecting model clients. Punishment promotes female cooperation, yielding direct foraging benefits to the male. This finding demonstrates empirically that third-party punishment can evolve via self-serving tendencies.When servicing clients, cleaners either cooperate by removing ectoparasites or cheat by taking a bite of mucus. Cleaners prefer to eat mucus (5) but risk clients terminating the interaction if they do (6). The conflict of interest between cleaner and client is less pronounced during inspections by cleaner pairs than during singleton inspections (7). Increased service quality during pair inspections was interpreted as resulting from female cooperation, both under natural conditions and in the laboratory where Plexiglas (acrylic plastic) plates serve as model clients. Larger males regularly chased smaller female partners if females caused clients to leave, particularly in the laboratory (7). This male behavior is peculiar because clients, not males, are the victims of biting females. Despite this fact, it is possible that male chasing could cause females to behave more cooperatively in future interactions. If males benefit personally through increased foraging success, then the males' behavior represents third-party punishment that evolves via self-regarding, rather than altruistic, tendencies.Cleaners were trained to feed off model clients (Plexiglas plates) containing two food types: preferred prawn and less-preferred fish flake (8). Eating prawn corresponded to cheating the client by eating mucus, whereas eating flake corresponded to cooperating by removing ectoparasites. Eating prawn resulted in the immediate removal of the plate. We replicated earlier results (7) that males more often chased females when the latter's behavior caused plate removal (Wilcoxon signedrank test, n = 8, V (rank sum of positive values of x = y) = 21, P = 0.036). After being chased, females were less likely to eat prawn again in the second plate presentation 60 s later (Wilcoxon signed-rank test, n = 8, V = 34, P = 0.030; Fig. 1A) and fed against their preference, eating a higher ratio of flake to prawns (Wilcoxon signedrank test, n = 8, V = 36, P = 0.008; Fig. 1B). This allowed males to increase their food intake in the second presentation (Wilcoxon signed-rank test, n = 8, V = 28, P = 0.02; Fig. 1C). Conversely, when chasing was prevented with a temporary partition, females that cheated in the first presentation were equally likely to cheat in the second one (Wilcoxon signed-rank test, n = 8, V = 11, P = 0.67; Fig. 1A) and did not eat a higher ratio of flake to prawn items (Wilcoxon signed-rank test, n = 8, V = 8, P = 0.35; Fig. 1B), a...

Punishment and spite, the dark side of cooperation

“…Policing in social insects is a special case since the destruction of eggs for the benefit of the remainder of the hive benefits the punishers indirectly through kin benefits (Ratnieks & Wenseleers 2008), a point that will be expanded upon in §4. In one experiment, male cleaner fish aggressed against female partners for 'cheating' by taking the preferred food from a plastic plate, resulting in the immediate removal of the common food source (Raihani et al 2010). As a result, the females were less likely to take the preferred food in subsequent trials.…”

“…As a result, the females were less likely to take the preferred food in subsequent trials. While Raihani et al's (2010) study was designed to make a point about third-party functional punishment, it was actually a test of second-party functional punishment since there was no third party, and since the punisher benefited directly by altering the behaviour of his partner to his benefit. While clients may benefit in natural settings, this study demonstrated that third-party benefits would be a by-product of a coercive strategy.…”

Reputation based on punishment rather than generosity allows for evolution of cooperation in sizable groups

“…Punishment can increase cooperation levels if there are opportunities to punish defectors, that is, decreasing a defector's immediate payoff at a personal immediate cost (Fehr & Gächter, 2002;Raihani et al, 2010;Raihani et al, 2012;Sigmund, 2007). Until recently, such costly punishment has been perceived as an evolutionary puzzle because punishers accept costs to harm others while third parties benefit from the increased cooperation levels (Dreber et al, 2008;Fehr & Gächter, 2002;Rankin et al, 2009;Sigmund, 2007;Wu et al, 2009).…”

Evidence for tactical concealment in a wild primate

“…However, punishment is rarely observed outside the context of human society 27 , mainly because most intraspecific aggression results in an immediate benefit for the aggressor, thereby qualifying as a form of direct competition 19,26 . A few studies have explicitly demonstrated the punishment of non-cooperative behaviour in birds 2 and fish 28 , but its scarcity in primates is surprising given the importance of punishment in human societies 25,27 . Further, punishment seldom leads to clear behavioural modifications (that is, increased cooperation or decreased competition) in the punished parties 29 , and there is some debate about the importance of behavioural modification in the evolution of punishment 30 .…”