A century of theories of balancing selection

Abstract:
Traits that affect organismal fitness are often very genetically variable. This genetic variation is vital for populations to adapt to their environments, but it is also surprising given that nature (after all) “selects” the best genotypes at the expense of those that fall short. Explaining the extensive genetic variation of fitness-related traits is thus a longstanding puzzle in evolutionary biology, with cascading implications for ecology, conservation, and human health. Balancing selection—an umbrella term for scenarios of natural selection that maintain genetic variation— is a century-old explanation to resolve this paradox that has gained recent momentum from genome-scale methods for detecting it. Yet evaluating whether balancing selection can, in fact, resolve the paradox is challenging, given the logistical constraints of distinguishing balancing selection from alternative hypotheses and the daunting collection of theoretical models that formally underpin this debate. Here, we track the development of balancing selection theory over the last century and provide an accessible review of this rich collection of models. We first outline the range of biological scenarios that can generate balancing selection. We then examine how fundamental features of genetic systems—including non-random mating between individuals, differences in ploidy, genetic drift, and different genetic architectures of traits— have been progressively incorporated into the theory. We end by linking these theoretical predictions to ongoing empirical efforts to understand the evolutionary processes that explain genetic variation.