The evolution of altruism and the serial rediscovery of the role of relatedness

Abstract

The genetic evolution of altruism (i.e., a behavior resulting in a net reduction of the survival and/or reproduction of an actor to benefit a recipient) once perplexed biologists because it seemed paradoxical in a Darwinian world. More than half a century ago, W. D. Hamilton explained that when interacting individuals are genetically related, alleles for altruism can be favored by selection because they are carried by individuals more likely to interact with other individuals carrying the alleles for altruism than random individuals in the population ("kin selection"). In recent decades, a substantial number of supposedly alternative pathways to altruism have been published, leading to controversies surrounding explanations for the evolution of altruism. Here, we systematically review the 200 most impactful papers published on the evolution of altruism and identify 43 evolutionary models in which altruism evolves and where the authors attribute the evolution of altruism to a pathway other than kin selection and/or deny the role of relatedness. An analysis of these models reveals that in every case the life cycle assumptions entail local reproduction and local interactions, thereby leading to interacting individuals being genetically related. Thus, contrary to the authors' claims, Hamilton's relatedness drives the evolution to altruism in their models. The fact that several decades of investigating the evolution to altruism have resulted in the systematic and unwitting rediscovery of the same mechanism is testament to the fundamental importance of positive relatedness between actor and recipient for explaining the evolution of altruism.

Keywords: Hamilton’s rule; altruism; evolution; kin selection; rediscovery.

Fig. 1.

Population structure and relatedness, reproduced from Hamilton (17), who discussed how limited dispersal induced by various population structures influences patterns of relatedness and thereby affects the evolution of social behavior. In the panmictic and viscous models, smaller dots indicate younger individuals, and arrows indicate parenthood. In the island and stepping-stone models, younger individuals are not shown because reproduction occurs within groups. Arrows indicate dispersal between groups. For the viscous, island, and stepping-stone models, locally interacting individuals are positively related under limited dispersal, and the local relatedness structure has been explored in the field of population genetics (, –21). The viscous model with continuous space is the most challenging to analyze and remains the least explored, yet it is probably the most realistic model for plant populations. Most of the papers rediscovering kin selection use either the island model (using groups of size $>$1 and with interactions occurring within groups) or the stepping-stone model (using “groups” composed of a single individual, represented as the node of a lattice structure; since migration links nodes, the population becomes a network with interactions occurring between neighboring nodes). Reprinted with permission from ref. .