Abstract
AbstractThere 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.
Highlights
There are many situations in nature where we expect traits to evolve but not necessarily for mean fitness to increase
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
Environmental change is often assumed to be absent when using the Price identity (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 fundamental theorem of natural selection (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
Summary
Fitness is one of the most important concepts in evolutionary biology. It represents how well an organism passes its genes onto the generation, such as how many surviving offspring it has. It is easy to find examples of evolution where average fitness is not increasing (i.e., evolution but no adaptation), which seems to contradict these fundamental theories. We reconcile this apparent paradox by considering that individuals can influence each other’s fitness through social interactions such as fighting or cooperating. In recognizing that an individual’s fitness is determined not just by their own genes, and by the genes of those individual with whom they interact, social evolution theory can reconcile an apparent paradox between two theoretical pillars of evolutionary biology
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