Origin of Eusociality: Back to Direct Fitness

The evolutionary origin of eusociality has also been explained as arising from a combination of factors that center on direct fitness, in which indirect fitness (kinship) plays no causal role, although it can be a consequence of eusocial organization (Nowak, Tar-nita, & Wilson, 2010). This view originates in empirical observations from both field and

Figure 11.13 A hypothesis of the evolution of eusociality based on direct fitness advanced by Nowak, Tarnita, and Wilson (2010).

laboratory studies, and it gives no special status to the haplodiploid system characterizing many of the eusocial species.

Figure 11.13 presents a series of hypothetical stages leading to the evolution of advanced eusocial organization of the type observed, for example, in hymenopteran insects. The first stage involves the formation of groups from an inseminated female that generates offspring which do not disperse, but stay together and fulfill nonreproductive functions, such as nest defense. All eusocial species share one feature: they all live in nests that require extensive construction or maintenance, that are actively defended from intruders, and that are close to food resources. This feature is true even for species that display a simple form of eusociality (e.g., some wasps, aphids). Nest defense is a grouping factor that provides for stability and allows for the overlap of generations.

The second stage involves the expression of traits that favor eusociality, but were not evolved for that function—preadaptations. For example, traits that favor nest building and division of labor can be seen as preadaptations. These traits occur under some conditions in solitary species. For example, some solitary bees exhibit division of labor when forced to live in pairs under laboratory conditions. This apparently arises from variation in the threshold to perform different activities and a tendency of individuals to switch away from activities already performed by a group member. Preadaptations then bias many species to eusociality.

The third stage involves the accumulation of alleles that promote eusociality. An example of this is a mutation that discourages dispersal of the adult offspring to build a new nest and deposit fertilized eggs. Such a genetic change would promote group stability. Additional genetic or epigenetic changes silencing some genes and triggered by environmental factors, such as nutrition (see Box 11.1), could be responsible for some anatomical and behavioral

Reproductive and Social Behavior 443 traits that differentiate sterile individuals from their queen (Yan, Simola, Bonasio, Liebig, Berger, & Reinberg, 2014).

The fourth stage involves the action of natural selection on genetic variations that are expressed as a result of group stability. Natural selection acts on the queen, but since all members of the colony share the genes, the colony can be viewed as a unit or superorganism, as envisioned by Darwin and others (Owen, 2014).

Finally, selection among colonies would explain the diversity and complexity of eusocial organizations. Up until the fourth stage in this hypothesis, the evolutionary origin of euso-ciality rests on direct selection. In this final stage, the idea of group selection is brought back. But the accumulation of genetically related individuals is considered a consequence of family members staying together, rather than a cause of eusociality.