Cooperation is subject to cheating strategies that exploit the benefits of cooperation without paying the fair costs, and it has been a major goal of evolutionary biology to explain the origin and maintenance of cooperation against such cheaters. Here, we report that cheater genotypes indeed coexist in field colonies of a social insect, the parthenogenetic ant Pristomyrmex punctatus. The life history of this species is exceptional, in that there is no reproductive division of labour: all females fulfil both reproduction and cooperative tasks. Previous studies reported sporadic occurrence of larger individuals when compared with their nest-mates. These larger ants lay more eggs and hardly take part in cooperative tasks, resulting in lower fitness of the whole colony. Population genetic analysis showed that at least some of these largebodied individuals form a genetically distinct lineage, isolated from cooperators by parthenogenesis. A phylogenetic study confirmed that this cheater lineage originated intraspecifically. Coexistence of cheaters and cooperators in this species provides a good model system to investigate the evolution of cooperation in nature.
How should females and males move to search for partners whose exact location is unknown? Theory predicts that the answer depends on what they know about where targets can be found, raising the question of how actual animals update their mate search patterns to increase encounter probability when conditions change. Here, we show that termites adaptively alternate between sexually monomorphic and dimorphic movements during mate search. When the location of potential mates was completely unpredictable, both sexes moved in straight lines to explore widely. In contrast, when the stray partner was at least nearby, males moved while females paused. Data-based simulations confirmed that these movements increase the rate of successful encounters. The context-dependent switch of search modes is a key to enhance random encounters.
Cooperation in biological, social, and economic groups is underpinned by public goods that are generated by group members at some personal cost. Theory predicts that public goods will be exploited by cheaters who benefit from the goods by not paying for them, thereby leading to the collapse of cooperation. This situation, described as the "public goods dilemma" in game theory, makes the ubiquity of cooperation a major evolutionary puzzle. Despite this generalization, the demonstration of genetic background and fitness effects of the public goods dilemma has been limited to interactions between viruses and between cells, and thus its relevance at higher levels of organismal complexity is still largely unexplored. Here we provide experimental evidence for the public goods dilemma in a social insect, the ant Pristomyrmex punctatus. In this species, all workers are involved in both asexual reproduction and cooperative tasks. Genetic cheaters infiltrate field colonies, reproducing more than the workers but shunning cooperative tasks. In laboratory experiments, cheaters outcompeted coexisting workers in both survival and reproduction, although a group composed only of cheaters failed to produce offspring. The operations of the public goods dilemma in P. punctatus showed a remarkable convergence with those in microbial societies, not only in fitness consequences but also in behavioral mechanisms. Our study reinforces the evolutionary impact of cheaters on diverse cooperative systems in the laboratory and in the field. social evolution | public goods game | social parasitism | self-organization | phenotypic plasticity
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