Where did the love come from? Inclusive fitness vs. group selection

Altruism is widespread in the animal world, yet it seems to conflict with the picture of nature “red in tooth and claw” often associated with Evolution. One solution to this apparent paradox is to remember that the unit of selection is never the individual itself but the genes  it carries. Thus, altruism may be explained if the altruist shares genes with the individual it helps in such a way that, while harming itself as an individual, it favors the spread of its genes. This idea of analyzing selection at the level of genes rather than the individual dates back to the 1930s, when Darwin’s theory and Mendelian genetics were first combined to form a unified framework now known as the neo-Darwinian synthesis.

Altruism is a common feature of animal behaviour. In this picture, a chimp mother helping another down a tree. Source: The Selfishness of Giving by Frans de Waal on Huffington Post.

Inclusive Fitness and Hamilton’s rule

But not until a few decades later, when D.W. Hamilton proposed his famous rule, was the idea integrated into evolutionary models. As Hamilton himself noted in his seminal 1964 paper: “With very few exceptions, the only parts of the theory of natural selection which have been supported by mathematical models admit no possibility of the evolution of any characters which are on average to the disadvantage of the individuals possessing them.” (Hamilton 1964) Early models focused on individual fitness without considering implications for relatives, with the notable exception of parental care. Filling this vacuum, Hamilton proposed a simple model which aimed to explain how self-harming social behavior could evolve. The basic idea is, again, to look at the effects of an action on the altruist’s “inclusive fitness” – i.e. on all the copies of its genes. To do this, one must add up the reproductive benefit () to each recipient, weighed by its genetic relatedness to the altruist (), and compare this benefit to the reproductive cost to the altruist (), yielding “Hamilton’s rule”: an altruistic action is selectively favored if . ( is usually formulated in one of two ways: as the probability that, for a randomly chosen locus, two individuals share the same allele by descent, or as the proportion of alleles common to both genotypes).

In formulating this rule, Hamilton did not intend to create a new theory distinct from natural selection. Rather, his model attempts to fully account for the genetic underpinning of natural selection. As has been amply noted in recent literature, much criticism of inclusive fitness theory (IFT) stems from the mistaken belief that inclusive fitness is distinct from “regular” natural selection. But before I describe further the controversy surrounding inclusive fitness, let us consider a competing, though not exclusive, explanation for the evolution of altruism: group selection.

Group selection: an alternative mechanism for the evolution of altruism

Group selection is the selection of altruistic traits resulting from the differential survival of entire groups of organisms. Three requirements must be met for group selection to happen: (1) the groups have to be reproductively isolated, at least to a degree; (2) the new altruistic trait must improve the chances of survival of the trait-carrying group relative to other groups; and (3) the gene that causes the trait must establishes itself first in a small group through genetic drift. The first two conditions are self-explanatory if we remember that the groups themselves must be the units of selection. As for the third, it can be understood with the use of an example borrowed from Maynard Smith. Consider (partly) reproductively isolated groups of Anubis baboons. Anubis baboons live in large troops; males must leave their troop to mate while females always remain in their native group. As a result, males are typically genetically far from other males, females, and all offspring beside their own, whereas females of the same troop are closely related. Note further that infanticide by unrelated adult male baboons is common. Suppose now that a mutation causes some females to protect the offspring of other females in their troop and that the mutant gene spreads through the group whose fitness increases as a result. Is group selection at play here? The example was chosen so that the first two conditions – reproductive isolation and differential extinction – are met. However, we have to explain how the altruistic trait spread through the group in the first place. Since the group is large, genetic drift (gene frequency changes due to random gene sampling at each generation) cannot be responsible for the gene’s spread. Instead, it is likely that the mutation increases the inclusive fitness of the altruistic female, giving it a selective advantage. Or, we can imagine that the apparently altruistic action in fact helps the defendant female through, say, reciprocal defense. Thus, when genetic drift does not the cause the trait’s initial spread, even if it eventually benefits the entire group, selection for altruism cannot be explained by group selection alone (Maynard Smith 1976).

Empirical tests

Inclusive fitness and group selection – at least as I understand them – both are logically consistent with natural selection and with each other. Yet, during the last decades, the two theories have split the scientific community into two warring camps, each holding tightly to a theory and denigrating the other, sometimes with rather “unscientific” ardor and partiality. The disagreement stems partly from a misunderstanding. In a recent paper highly critical of inclusive fitness, Nowak et al. argue that IFT is a superfluous construct , an “abstract entreprise” divorced from natural selection. They claim that inclusive fitness theory (1) only considers the direct effects of altruistic actions while ignoring all retroactive effects of the recipients on the actor; (2) ignores all synergistic effects and assumes that the effects of the action are additive; (3) can only be applied to special types of population structure, namely static structures (fixed interactions between individuals) and “0 or 1” dynamic structures (where individuals either interact or don’t) (Nowak et al. 2010). While particular models may be rightful targets of this criticism, inclusive fitness itself is not. These restrictions are features of (necessarily) simplified models – especially those in textbooks – not of the theory as such.

Group selection and kin selection both being compatible with natural selection, we can only arbitrate between them by comparing their empirical merits. One domain in which this has been done is the study of eusocial animals. Eusociality – a phenomenon observed primarily among insects- occurs when labor, defense and reproduction are divided among castes in a colony. Eusociality involves altruism since all workers and warriors sacrifice their direct reproductive potential to support the reproducing caste. Early inclusive fitness theorists posited that in colonies with non-overlapping generations, eusociality should be more prominent where sibling-relatedness is high because in that case the inclusive fitness benefits of altruism are greater. Some theorists predicted, for instance, that eusociality is more widespread in insects exhibiting haplodiploidy – a type of sex determination whereby unfertilized eggs give birth to males and fertilized eggs, to females. Since they inherit the integrity of their father’s genotype, haplodiploid sisters share a large portion of their genes. Hence, altruistic and eusocial behavior should be more likely to evolve in haplodiploids.

Or so theorists claimed, until data collected in the last decades proved them wrong: haplodiploidy and eusociality are not statistically correlated. Nowak et al. claimed that this failure invalidates IFT, whose predictive results, they say, have been meager. But in doing so, they once again threw the baby with the bathwater, so to speak (Nowak et al. 2010). Haplodiploidy aside, IFT explains a wide range of phenomena. Shortly after Nowak et al.’s attack on the IFT, 137 authors (!) wrote a scathing response that drew attention to IFT’s predictive and explanatory power. For instance, colonies with single queens are statistically more likely to be eusocial, probably for the same reason that haplodiploidy was expected to favor eusociality: in single-queen colonies siblings share on average a greater portion of their genotypes (Abbot et al. 2011). But why then is haplodiploidy, unlike single-queen colony structure, not correlated with eusociality? One possible reason is that the inclusive fitness benefits of altruism are overwhelmed by competition since, when siblings compete, the reproductive cost () of altruistic behavior may exceed its inclusive benefits () (Mulder 2007).

In short, group selection and inclusive fitness are both ways to account for the genetic basis of natural selection. As such, neither is a separate framework competing with classical evolution, and both may provide useful explanations and predictions in understanding altruism – as has been amply shown for inclusive fitness. More research is needed, however, to assess their relative importance in the evolution of altruistic behavior.

References

Abbot, P., Abe, J., Alcock, J., Alizon, S., Alpedrinha, J. A., Andersson, M., … & Gardner, A. (2011). Inclusive fitness theory and eusociality. Nature, 471(7339): E1-E4.

Hamilton, W. W. (1964). The genetical evolution of social behaviour 1. J. Theoret. Biol., 7: 1-16.

Maynard Smith, J. (1976). Group selection. Quarterly Review of Biology, 51(2): 277-283.

Mulder, M. B. (2007). Hamilton’s rule and kin competition: The kipsigis case. Evolution and Human Behavior, 28: 299-312.

Nowak M.A., Tarnita C.E. & Wilson E.O. (2010). The evolution of eusociality, Nature, 466 (7310) 1057-1062. DOI: 10.1038/nature09205