Local negative frequency-dependence can decrease global coexistence in fragmented populations

Abstract

Most biological populations are rich in diversity, and negative frequency-dependent (NFD) selection is a well-established mechanism thought to underlie this stable coexistence of multiple variants. Recent studies confirm its widespread presence at local spatial scales, however it remains unclear whether these local-scale dynamics are sufficient to maintain biodiversity across larger, landscape-level scales. While prior theoretical work has found that local NFD selection can indeed promote global coexistence, these studies only analyzed contiguous landscapes. In contrast, many ecosystems are not contiguous, but rather spatially fragmented or exhibit spatial variation in the local carrying capacity. Using a theoretical model based on the classic island framework, we show that in fragmented populations, NFD selection can paradoxically reduce coexistence and shorten fixation times, relative to neutrality. Fragmentation also produces a non-monotonic relationship between fixation time and population size, with diversity lowest at intermediate scales, in contrast to the classical species-area relationship. We show that these results persist in a multispecies modeling framework. We also develop a statistical test to detect whether NFD selection suppresses coexistence in fragmented systems, and apply it to a presence-absence dataset of avian species in the Ryukyu Islands, finding evidence that NFD selection indeed reduces biodiversity in this case. Together, our findings suggest that fragmentation can undermine the stabilizing effects of NFD selection, calling into question its generality as a mechanism for maintaining biodiversity in heterogeneous landscapes. Broader significanceAs human activities increasingly fragment once-continuous habitats, it becomes ever more critical to understand how these changes impact biodiversity. Negative frequency-dependent (NFD) selection, a key mechanism promoting coexistence, is well known for preserving genetic and species diversity in well-mixed and spatially continuous populations. Using a theoretical model of a subdivided population, we show that NFD selection can actually accelerate extinctions and erode biodiversity, if the population is fragmented. This counterintuitive result arises because habitat fragmentation disrupts the alignment between the local scale of ecological interactions and the broader landscape structure of the habitat. When local frequency-dependent dynamics no longer scale up across the landscape, their stabilizing effect is lost. Our findings suggest that, in fragmented environments, biodiversity may be better preserved under neutral dynamics or even weak directional selection, than under NFD selection.