Prudent males, group adaptation, and the tragedy of the commons

For almost five decades three threads have coexisted in the evolutionary and ecological literature, with their links only recently becoming visible and some of them still not properly addressed. These are the levels of selection debate, the metaphor of the tragedy of the commons, and the evolutionary study of sexual conflict. We analyze the eco-evolutionary dynamics of a curious system where an asexual all-female fish species (the Amazon molly Poecilia formosa) requires sperm from other species as a developmental trigger, without utilizing the genes from sperm. The dynamics of such a system bear strong resemblance to host-parasite dynamics, and populations of the sexual 'host' species persist much better if males avoid mating with Amazons. However, such avoidance may compromise their current mating success, and if this is the case, prudent mating becomes an altruistic trait that helps to keep an accumulating problem of a competing species at bay, and Amazon-free space can be seen to form a common good that a population should maintain for future generations. A model shows that the evolution of altruistic mating restraint is possible but selection for short-term gains means that it will remain less than perfect. This helps to explain why the anomalous gynogenetic system can persist, but it also raises questions about what kinds of traits can be classified as adaptations when optimization is not perfect and traits evolve to achieve short-term goals better than long-term performance. Contributing to the levels of selection debate, we encourage researchers to study the implications of the different timescales involved in the eco-evolutionary process.