Genetic and phenotypic variation exhibit both predictable and stochastic patterns across an intertidal fish metapopulation

Interactions among selection, gene flow, and drift affect the trajectory of adaptive evolution. In natural populations, the direction and magnitude of these processes can be variable across different spatial, temporal, or ontogenetic scales. Consequently, variability in evolutionary processes affects the predictability or stochasticity of microevolutionary outcomes. We studied an intertidal fish, Bathygobius cocosensis (Bleeker 1854), to understand how space, time, and life stage structure genetic and phenotypic variation in a species with potentially extensive dispersal and a complex life cycle (larval dispersal preceding benthic recruitment). We sampled juvenile and adult life stages, at three sites, over three years. Genome-wide SNPs uncovered a pattern of chaotic genetic patchiness, that is, weak-but-significant patchy spatial genetic structure that was variable through time and between life stages. Outlier locus analyses suggested that targets of spatially divergent selection were mostly temporally variable, though a significant number of spatial outlier loci were shared between life stages. Head shape, a putatively ecologically responsive (adaptive) phenotype in B. cocosensis, also exhibited high temporal variability within sites. However, consistent spatial relationships between sites indicated that environmental similarities among sites may generate predictable phenotype distributions across space. Our study highlights the complex microevolutionary dynamics of marine systems, where consideration of multiple ecological dimensions can reveal both predictable and stochastic patterns in the distributions of genetic and phenotypic variation. Such considerations likely apply to species that possess short, complex life cycles, have large dispersal potential and fecundities, and that inhabit heterogeneous environments.