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The revival of group selection is a result of better models and experimental studies showing it is indeed possible, as well as the realisation by biologists that today’s individuals are yesterday’s groups. In addition, it has become clear that the supposed alternative explanations for the evolution of prosocial behaviour are actually equivalent to group selection.

The evidence

The rejection of group selection was based on the claim that, in practice, selection within groups always beats selection between groups. However, recent studies have shown that traits can evolve on the strength of between-group selection, despite being disadvantageous for individuals within each group.

Take the water strider Remigis aquarius, an insect species that skates on the surface of quiet streams. Males vary greatly in their aggressiveness toward females, and lab studies by Omar Tonsi Eldakar and colleagues, including me, show that within any group, aggressive males outcompete non-aggressive males for females.

However, the aggressive males also prevent females from feeding and can injure them, which results in a group with lots of aggressive males producing fewer offspring than groups with fewer aggressive males. Variation among groups is magnified by females fleeing groups containing lots of aggressive males and aggregating in groups with non-aggressive males. So our studies show that between-group selection is essential for maintaining non-aggressive males in the population ().

In another experiment, a team of microbiologists headed by Benjamin Kerr at the University of Washington in Seattle grew E. coli in wells on plates. They then infected some of them with a virus, and mimicked the natural spread of viruses by using robotic pipettes to transfer them between wells.

The team found that in some circumstances, a “prudent”, slow-growing strain of the virus was more successful than a “rapacious”, fast-growing strain. The rapacious strain often killed off all the bacteria in a well – and therefore itself – before it had a chance to spread. The prudent strain persisted for longer and so was more likely to get a chance to colonise other wells.

In this way, the prudent strain could remain in the population even though it was always outcompeted by the rapacious strain when both were present in a single well. In other words, it was only on the strength of between-group selection that the prudent strain survived ().

The conditions of this experiment closely resemble a scenario proposed by Vero C. Wynne-Edwards in the 1960s for the evolution of reproductive restraint in many species. Such restraints might not evolve in all species, but as this experiment shows, it is plausible that they can evolve in some species in some circumstances.

These two experiments involve very different spatial and temporal scales, but they embody the key problem and simple solution of group selection: the traits that benefit the whole group are not advantageous for individuals within the group and so require an additional layer of natural selection to evolve.

Major transitions

Until the 1970s, evolution was thought to take place entirely on the basis of the accumulation of mutations over many generations. Then biologist Lynn Margulis proposed that complex cells did not evolve by small mutational steps from bacterial cells, but from symbiotic associations of different kinds of bacteria that became higher level organisms in their own right.

In the 1990s, evolutionary biologists John Maynard Smith and Eors Szathmary proposed that similar major transitions occurred throughout the history of life, including the evolution of the first cells, the advent of multicellular organisms and the development of social insect colonies (see diagram). They even suggested it could explain the origin of life, with groups of cooperating molecular reactions coming together to create the first life forms. The realisation that evolution takes place not only by small mutational steps but also by groups of organisms turning into higher-level organisms represents one of the most profound developments in evolutionary thought. Today’s individuals are yesterday’s groups.

For a major evolutionary transition to occur, there has to be a shift in the balance between within-group and between-group selection. A group can only turn into an individual when between-group selection is the primary evolutionary force, and this in turn can happen only when mechanisms evolve that suppress selection within groups. The rules of meiosis, for example, ensure that all genes on the chromosomes have an equal chance of being represented in the gametes. If genes can’t succeed at the expense of each other, then the only way to succeed is collectively as a group.

“A group can only evolve into an individual when between-group selection is the primary force”

Major evolutionary transitions are rare events in the history of life but they have momentous consequences, as the new super-organisms become ecologically dominant. Eusociality in insects only originated about a dozen times – including in ants, bees, wasps and termites – but insect colonies comprise well over half the biomass of all insects.

These transitions are never complete as selection within groups is only suppressed, not eliminated. Some genes do manage to bias the rules of meiosis in their favour. Increasingly, cancer is studied as an evolutionary process that takes place within individuals, causing some genes to succeed at the expense of others, with tragic results for the group as a whole.

Selfish genes

The rejection of group selection in the 1960s meant biologists had to come up with alternative theories to explain the evolution of social adaptations. Several were put forward, including inclusive fitness theory – also known as kin selection – selfish gene theory and evolutionary game theory. In retrospect, all of these theories can be shown to invoke group selection after all.

William D. Hamilton, who came up with inclusive fitness theory in the 1960s, was among the first to realise this after encountering the work of theoretical biologist George Price in the 1970s. Hamilton’s formula calculated when an altruistic gene evolves in the whole population but did not keep track of what happens in any particular group. In contrast, Price’s formula divided evolution in the whole population into within and between-group components. When Hamilton viewed his own theory through the lens of Price’s formulation, he saw that altruism is usually a disadvantage within groups and evolves only by virtue of between-group selection, exactly as Darwin envisioned.

This is true even when groups are composed of relatives. Group selection can occur only when there is variation among groups, and since groups of relatives are more likely to differ from each other than groups of unrelated individuals, relatedness increases the strength of between-group selection compared with within-group selection.

As Hamilton recalls his realisation: “Through a ‘group-level’ extension of [Price’s] formula I now had a far better understanding of group selection and was possessed of a far better tool for all forms of selection acting at one level or at many than I had ever had before.” Unfortunately, other biologists did not share this insight: while Hamilton’s 1960s work was much cited, his revised formulation was largely ignored.

Recently, though, it has become clear that all evolutionary theories of social behaviour implicitly assume that social interactions take place in groups that are small compared with the population as a whole. Also, that the prosocial behaviours variously labelled “cooperation” or “altruism” are disadvantageous to individuals and evolve only by virtue of the differential contribution of groups to the total gene pool. In other words, each theory relies upon the simple logic of multilevel selection.

The reason that this was not obvious from the beginning is because these theories only tracked what evolves in the whole population without simultaneously tracking natural selection within single groups. It is impossible to evaluate whether group selection needs to be invoked without tracking natural selection at each relevant level of the biological hierarchy.

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