Frequency-dependent selection

Frequency-dependent selection describes an evolutionary process where the reproductive success (fitness) of a particular trait or strategy is not fixed, but instead varies as a function of how common or rare that trait is within the population. When a trait's fitness increases as it becomes rarer, it is known as negative frequency-dependent selection, which tends to maintain polymorphism. Conversely, positive frequency-dependent selection occurs when a trait's fitness increases as it becomes more common, typically leading to the fixation of that trait and the loss of alternatives.

Origins and Mechanisms

The concept of frequency-dependent selection has roots in early population genetics and game theory. Fisher (1930) recognized that the 1:1 sex ratio could be maintained by frequency-dependent selection, as the rarer sex would confer a reproductive advantage to parents producing it. Later, Maynard Smith and Price (1973) formalized the application of game theory to evolutionary biology with the concept of the Evolutionarily Stable Strategy (ESS). An ESS is a strategy that, if adopted by a population, cannot be invaded by any alternative strategy; it is often maintained by frequency-dependent selection. If a mutant strategy arises, its success depends on its frequency relative to the prevailing ESS.

Negative frequency-dependent selection is particularly important for understanding the persistence of genetic and phenotypic variation. When a strategy is rare, it enjoys a fitness advantage, allowing it to increase in frequency. As it becomes more common, its advantage diminishes, or even becomes a disadvantage, which then favors alternative, rarer strategies. This dynamic creates a stable equilibrium where multiple strategies coexist within a population. This mechanism is distinct from other forms of balancing selection, such as heterozygote advantage, which maintains variation at a specific locus regardless of its frequency.

Positive frequency-dependent selection, while less commonly associated with maintaining variation, plays a role in phenomena like Batesian mimicry, where the fitness of a palatable mimic increases with its resemblance to a common, unpalatable model. It can also drive traits to fixation, as the benefits of a trait amplify with its prevalence, leading to a runaway effect until the alternative is eliminated.

Behavioral and Social Applications

Frequency-dependent selection is a powerful explanatory tool in evolutionary psychology and behavioral ecology, particularly for understanding the maintenance of diverse behavioral strategies within a species. Many social interactions involve payoffs that depend on the relative frequencies of different strategies in a population.

One classic example is the 'Hawk-Dove' game (Maynard Smith and Price, 1973), which models aggressive interactions. 'Hawks' always fight aggressively, while 'Doves' display and retreat if challenged. The fitness of each strategy depends on the frequency of the other. If Hawks are rare, they do well because they often encounter Doves and win. If Hawks are common, they frequently encounter other Hawks, leading to costly fights. Conversely, Doves do poorly against Hawks but avoid injury by retreating. This dynamic can lead to a stable polymorphism where both Hawk and Dove strategies (or a mixed strategy) coexist, with their frequencies determined by the costs and benefits of fighting.

Another application is in the study of cooperation and defection. In scenarios like the Prisoner's Dilemma, the optimal strategy for an individual often depends on the strategies adopted by others in the population. The success of a cooperator or a defector can be frequency-dependent, potentially leading to the maintenance of both strategies under certain conditions, especially when interactions are repeated or occur in structured populations (Axelrod and Hamilton, 1981).

Sex differences in mating strategies also show evidence of frequency dependence. For instance, some theories suggest that male mating strategies, such as investing in long-term pair bonds versus pursuing multiple short-term matings, might be maintained by frequency-dependent selection (Gangestad and Simpson, 2000). If one strategy becomes too common, its benefits may diminish, favoring the alternative. For example, if all males pursue short-term matings, the competition for fertile females might become so intense that the fitness returns for a male investing in parental care increase.

Critiques and Nuances

While frequency-dependent selection provides a robust framework, its application requires careful consideration of the specific costs and benefits associated with different strategies. Critics sometimes point out that identifying the precise fitness functions and demonstrating their frequency dependence empirically can be challenging. Many behavioral traits are complex and influenced by multiple genes and environmental factors, making it difficult to isolate the effects of frequency dependence.

Furthermore, the concept of an ESS, while useful, assumes that strategies are genetically determined and fixed. In reality, individuals may adopt mixed strategies or adjust their behavior based on social learning or environmental cues. This behavioral plasticity adds layers of complexity to frequency-dependent models. Laland and Brown (2002) emphasize the importance of cultural transmission and learning in shaping behavioral frequencies, which can interact with genetic frequency-dependent processes.

Despite these complexities, frequency-dependent selection remains a cornerstone of evolutionary theory, providing a powerful explanation for the maintenance of behavioral and genetic diversity, particularly in contexts where social interactions and relative fitness payoffs are paramount.