Footprints of local adaptation span hundreds of linked genes in the Atlantic silverside genome

The study of local adaptation in the presence of ongoing gene flow is the
study of natural selection in action, revealing the functional genetic
diversity most relevant to contemporary pressures. In addition to
individual genes, genome-wide architecture can itself evolve to enable
adaptation. Distributed across a steep thermal gradient along the east
coast of North America, Atlantic silversides (Menidia menidia) exhibit an
extraordinary degree of local adaptation in a suite of traits, and the
capacity for rapid adaptation from standing genetic variation, but we know
little about the patterns of genomic variation across the species range
that enable this remarkable adaptability. Here we use low-coverage,
whole-transcriptome sequencing of Atlantic silversides sampled along an
environmental cline to show marked signatures of divergent selection
across a gradient of neutral differentiation. Atlantic silversides sampled
across 1,371 km of the southern section of its distribution have very low
genome-wide differentiation (median FST=0.006 across 1.9 million
variants), consistent with historical connectivity and observations of
recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs)
are nearly fixed (FST>0.95) for alternate alleles. Highly
differentiated SNPs cluster into four tight linkage disequilibrium blocks
(LD) that span hundreds of genes and several megabases. Variants in these
LD blocks are disproportionately non-synonymous and concentrated in genes
enriched for multiple functions related to known adaptations in
silversides, including variation in lipid storage, metabolic rate, and
spawning behavior. Elevated levels of absolute divergence and demographic
modeling suggest selection maintaining divergence across these blocks
under gene flow. These findings represent an extreme case of heterogeneity
in levels of differentiation across the genome, and highlight how gene
flow shapes genomic architecture in continuous populations. Locally
adapted alleles may be common features of populations distributed along
environmental gradients, and will likely be key to conserving variation to
enable future responses to environmental change.