Selection over small and large spatial scales in the face of high gene flow

Local adaptation represents the balance of selection and gene flow.
Increasingly, studies find that adaptation can occur on spatial scales
much smaller than the scale of dispersal, resulting in balanced
polymorphisms within populations. However, in many cases we lack
information on how this microgeographic adaptation might facilitate or
hinder larger scale environmental heterogeneity, for example across
latitude. Marine systems present a special case, as many marine species
have high dispersal capacity so that dispersal ‘neighborhoods’ may
encompass environmental heterogeneity over both extremely small and
extremely large spatial scales. Here, we leverage fine-scale sampling
across the California range of the Pacific purple urchin
(Strongylocentrotus purpuratus), a species with previous evidence of both
local adaptation and extremely high gene flow. We find that despite
complete absence of neutral population structure, satellite-based sea
surface temperature and tidal zone drive genetic differences among
populations, suggesting that balanced polymorphisms can lead to adaptation
across both large scale (latitudinal) and small scale (subtidal v.
intertidal) scales. In fact, some of the same genetic variants
differentiate populations at both spatial scales, potentially because both
environmental parameters are related to temperature. Further, we find that
genes that are expressed at a single tissue or life history stage are more
divergent than expected across both latitudinal and tidal zone
comparisons, suggesting that these genes have specific functions that
might generate phenotypic variation important for local adaptation.
Together these results suggest that even in populations with little
population structure,  genetic variation can be sorted across
even small spatial scales, potentially resulting in local adaptation
across a complex environmental mosaic.