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Selection on standing genetic variation may be effective enough to allow for adaptation to distinct niche environments within a single generation. Minor allele frequency changes at multiple, redundant loci of small effect can produce remarkable phenotypic shifts. Yet, demonstrating rapid adaptation via polygenic selection in the wild remains challenging. Here we harness natural replicate populations that experience similar selection pressures and harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus that inhabits marine estuaries characterized by high environmental heterogeneity. We identify 10,861 single nucleotide polymorphisms in F. heteroclitus that belong to a single, panmictic population yet reside in environmentally distinct niches (one coastal basin and three replicate tidal ponds). By sampling at two time points within a single generation, we quantify both allele frequency change within as well as spatial divergence among niche subpopulations. We observe few individually significant allele frequency changes yet find that the "number" of moderate changes exceeds the neutral expectation by 10-100%. We find allele frequency changes to be significantly concordant in both direction and magnitude among all niche subpopulations, suggestive of parallel selection. In addition, within-generation allele frequency changes generate subtle but significant divergence among niches, indicative of local adaptation. Although we cannot distinguish between selection and genotype-dependent migration as drivers of within-generation allele frequency changes, the trait/s determining fitness and/or migration likelihood appear to be polygenic. In heterogeneous environments, polygenic selection and polygenic, genotype-dependent migration offer conceivable mechanisms for within-generation, local adaptation to distinct niches., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

It has been suggested that adaptive evolution on ecological timescales shapes communities. However, adaptation among environments relies on isolation or large selection coefficients that exceed migration effects. This reliance is tempered if adaptation is polygenic-does not depend on one allele completely replacing another but instead requires small allele frequency changes at many loci. Thus, whether individuals can evolve adaptation to fine-scale habitat variation (for example, microhabitats) is not resolved. Here we analyze the genetic divergence of the teleost fish, Fundulus heteroclitus, among microhabitats that are <200 m apart in three separate saltmarshes using 4741 single-nucleotide polymorphisms (SNPs). Among these SNPs, 1.3-2.3% have large and highly significant differences among microhabitats (mean F ST =0.15; false discovery rate ⩽1%). The divergence among microhabitats for these outlier SNPs is larger than that among populations, exceeds neutral expectation and indicates surprising population structure among microhabitats. Thus, we suggest that polygenic selection is surprisingly effective in altering allele frequencies among many different SNPs that share similar biological functions in response to environmental and ecological differences over very small geographic distances. We acknowledge the evolutionary difficulty of large genetic divergence among well-connected habitats. Therefore, these studies are only the first step to discern whether natural selection is responsible and capable of effecting genetic divergence on such a fine scale.