Meta-analytical evidence for frequency-dependent selection across the tree of life.

Explaining the maintenance of genetic variation in fitness-related traits within populations is a fundamental challenge in ecology and evolutionary biology. Frequency-dependent selection (FDS) is one mechanism that can maintain such variation, especially when selection favours rare variants (negative FDS). However, our general knowledge about the occurrence of FDS, its strength and direction remain fragmented, limiting general inferences about this important evolutionary process. We systematically reviewed the published literature on FDS and assembled a database of 747 effect sizes from 101 studies to analyse the occurrence, strength, and direction of FDS, and the factors that could explain heterogeneity in FDS. Using a meta-analysis, we found that overall, FDS is more commonly negative, although not significantly when accounting for phylogeny. An analysis of absolute values of effect sizes, however, revealed the widespread occurrence of modest FDS. However, negative FDS was only significant in laboratory experiments and non-significant in mesocosms and field-based studies. Moreover, negative FDS was stronger in studies measuring fecundity and involving resource competition over studies using other fitness components or focused on other ecological interactions. Our study unveils key general patterns of FDS and points in future promising research directions that can help us understand a long-standing fundamental problem in evolutionary biology and its consequences for demography and ecological dynamics.

Predator mass mortality events restructure food webs through trophic decoupling.

Predators have a key role in structuring ecosystems1-4. However, predator loss is accelerating globally4-6, and predator mass-mortality events7 (MMEs)-rapid large-scale die-offs-are now emblematic of the Anthropocene epoch6. Owing to their rare and unpredictable nature7, we lack an understanding of how MMEs immediately impact ecosystems. Past predator-removal studies2,3 may be insufficient to understand the ecological consequences of MMEs because, in nature, dead predators decompose in situ and generate a resource pulse8, which could alter ensuing ecosystem dynamics by temporarily enhancing productivity. Here we experimentally induce MMEs in tritrophic, freshwater lake food webs and report ecological dynamics that are distinct from predator losses2,3 or resource pulses9 alone, but that can be predicted from theory8. MMEs led to the proliferation of diverse consumer and producer communities resulting from weakened top-down predator control1-3 and stronger bottom-up effects through predator decomposition8. In contrast to predator removals alone, enhanced primary production after MMEs dampened the consumer community response. As a consequence, MMEs generated biomass dynamics that were most similar to those of undisturbed systems, indicating that they may be cryptic disturbances in nature. These biomass dynamics led to trophic decoupling, whereby the indirect beneficial effects of predators on primary producers are lost and later materialize as direct bottom-up effects that stimulate primary production amid intensified herbivory. These results reveal ecological signatures of MMEs and demonstrate the feasibility of forecasting novel ecological dynamics arising with intensifying global change.

Interactions between fitness components across the life cycle constrain competitor coexistence.

Numerous mechanisms can promote competitor coexistence. Yet, these mechanisms are often considered in isolation from one another. Consequently, whether multiple mechanisms shaping coexistence combine to promote or constrain species coexistence remains an open question. Here, we aim to understand how multiple mechanisms interact within and between life stages to determine frequency-dependent population growth, which has a key role stabilizing local competitor coexistence. We conducted field experiments in three lakes manipulating relative frequencies of two Enallagma damselfly species to evaluate demographic contributions of three mechanisms affecting different fitness components across the life cycle: the effect of resource competition on individual growth rate, predation shaping mortality rates, and mating harassment determining fecundity. We then used a demographic model that incorporates carry-over effects between life stages to decompose the relative effect of each fitness component generating frequency-dependent population growth. This decomposition showed that fitness components combined to increase population growth rates for one species when rare, but they combined to decrease population growth rates for the other species when rare, leading to predicted exclusion in most lakes. Because interactions between fitness components within and between life stages vary among populations, these results show that local coexistence is population specific. Moreover, we show that multiple mechanisms do not necessarily increase competitor coexistence, as they can also combine to yield exclusion. Identifying coexistence mechanisms in other systems will require greater focus on determining contributions of different fitness components across the life cycle shaping competitor coexistence in a way that captures the potential for population-level variation.

Predators weaken prey intraspecific competition through phenotypic selection.

Predators have a key role shaping competitor dynamics in food webs. Perhaps the most obvious way this occurs is when predators reduce competitor densities. However, consumption could also generate phenotypic selection on prey that determines the strength of competition, thus coupling consumptive and trait-based effects of predators. In a mesocosm experiment simulating fish predation on damselflies, we found that selection against high damselfly activity rates - a phenotype mediating predation and competition - weakened the strength of density dependence in damselfly growth rates. A field experiment corroborated this finding and showed that increasing damselfly densities in lakes with high fish densities had limited effects on damselfly growth rates but generated a precipitous growth rate decline where fish densities were lower - a pattern expected because of spatial variation in selection imposed by predation. These results suggest that accounting for both consumption and selection is necessary to determine how predators regulate prey competitive interactions.