- “a gene for (altruism) is favored when the altruism sufficiently benefits relatives carrying the gene.”
- “social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches”
- “reproductive altruism could evolve if it increased the worker’s inclusive fitness, which included effects that it had on increasing the fitness of its relatives”
- “One advantage of inclusive fitness thinking is that it induces researchers to think of (individuals) as agents being selected to get better outcomes (higher inclusive fitness) using whatever information is available to them.”
The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene.
Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness.
Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false…The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values…Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection.
This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.
The evolution of sterile worker castes in social insects has fascinated biologists ever since Darwin; how can selection favor a trait that decreases reproductive fitness? W. D. Hamilton solved this dilemma in the 1960s with a theory showing that reproductive altruism could evolve if it increased the worker’s inclusive fitness, which included effects that it had on increasing the fitness of its relatives. This solution to a crucial evolutionary problem, sometimes called kin selection, was challenged in a recent paper. The paper generated much controversy, but no one has contested its new theoretical model of the evolution of eusociality, which appeared to overturn much of what was previously thought to be true from kin selection theory. Here we examine this model in greater depth, showing that its apparently novel conclusions are overgeneralized from narrow and often inappropriate assumptions. Instead, this modeling strategy yields results that confirm important insights from kin selection and inclusive fitness, such as the importance of relatedness and the existence of conflicts in social insect colonies.
The eusocial insects have occupied an important place in biology because of their extraordinary levels of cooperation. In ants, termites, some bees, some wasps, and a few other taxa, certain individuals, called workers, give up their own reproduction in order to help others reproduce. Darwin was vexed over the question of how such reproductive altruism evolves or indeed how any traits of sterile workers evolve, but he believed that such sterility was due to some form of selection at the family level or at the group level.
Hamilton provided the first rigorous treatment of this idea, with a key insight being the importance of genetic relatedness:
- A conditional gene causing a worker to give up reproduction could be favored if it provided sufficient help to a relative who would share that gene at above-random levels
- He showed that this process, which became known as kin selection, could be analyzed by summing up an actor’s fitness effects, each multiplied by the actor’s relatedness to the individual receiving the fitness effect
- When this sum, called the inclusive fitness effect, is positive, the trait should be favored by selection. For giving up one’s reproduction (fitness cost c) to benefit other individuals (total fitness gain b) related by r, the inclusive fitness condition is −c + rb > 0.
Kin selection and inclusive fitness became the dominant modes of thinking about the evolution of eusocial insects, and their success in this area has led to them being applied to many other problems in social evolution. Recently, this paradigm was criticized by Nowak et al., who argued that inclusive fitness was an inaccurate and unnecessary method and that kin selection was not a very useful way to think about social evolution….
… We take causality to mean that variation in relatedness leads to variation in the likelihood of evolving eusociality…
Second, whereas inclusive fitness theory has emphasized that cooperation occurs in the face of potential and actual conflicts among colony members with different interests….
Whatever view of causality is taken, it is important to be clear that the Nowak et al.  modeling strategy is just like others in showing that higher relatedness is an important factor promoting higher cooperation.
… It is a longstanding result of inclusive fitness theory that parents and offspring are agents with different interests that can be in conflict… In particular, in the eusociality context, inclusive fitness predicts that offspring will be selected to help their mothers under a narrower range of conditions than the mothers would favor (eusociality evolves more readily if mothers control the helping of their offspring)… mothers favor helping by their offspring under a much broader range of conditions than the offspring themselves favor, except when mothers and offspring are genetically identical .
… One advantage of inclusive fitness thinking is that it induces researchers to think of (individuals) as agents being selected to get better outcomes (higher inclusive fitness) using whatever information is available to them…“