Polygenic selection within a single generation leads to subtle divergence among ecological niches

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 which 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.