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

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 and the Price identity. The consideration of indirect genetic effects 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. While transmission bias in the Price identity is often assumed to be absent, here we show that explicitly considering indirect genetic effects as a form of transmission bias for fitness has several benefits: 1) it makes clear how traits can evolve while mean fitness remains stationary, 2) it reconciles the fundamental theorem of natural selection 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) its 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 indirect genetic effects 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.