Indirect genetic effects clarify how traits can evolve even when fitness does not

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Abstract
There are many situations in nature where we expect traits to evolve but not necessarily for mean fitness to increase. However, these scenarios are hard to reconcile simultaneously with Fisher's fundamental theorem of natural selection (FTNS) and the Price identity (PI). The consideration of indirect genetic effects (IGEs) on fitness reconciles these fundamental theorems with the observation that traits sometimes evolve without any adaptation by explicitly considering the correlated evolution of the social environment, which is a form of transmission bias. Although environmental change is often assumed to be absent when using the PI, here we show that explicitly considering IGEs as change in the social environment with implications for fitness has several benefits: (1) it makes clear how traits can evolve while mean fitness remains stationary, (2) it reconciles the FTNS with the evolution of maladaptation, (3) it explicitly includes density-dependent fitness through negative social effects that depend on the number of interacting conspecifics, and (4) it allows mean fitness to evolve even when direct genetic variance in fitness is zero, if related individuals interact and/or if there is multilevel selection. In summary, considering fitness in the context of IGEs aligns important theorems of natural selection with many situations observed in nature and provides a useful lens through which we might better understand evolution and adaptation.
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