Genetic population structure constrains local adaptation in sticklebacks

Repeated and independent adaptation to specific environmental conditions
from standing genetic variation is common. However, if genetic variation
is limited, the evolution of similar locally adapted traits may be
restricted to genetically different and potentially less optimal solutions
or prevented from happening altogether. Using a quantitative
trait locus (QTL) mapping approach, we identified the genomic regions
responsible for the repeated pelvic reduction (PR) in three crosses
between nine-spined stickleback populations expressing full and reduced
pelvic structures. In one cross, PR mapped to linkage group 7 (LG7)
containing the gene Pitx1, known to control pelvic reduction also
in the three-spined stickleback. In the two other crosses, PR was
polygenic and attributed to ten novel QTL, of which 90% were unique to
specific crosses. When screening the genomes from 27 different populations
for deletions in the Pitx1 regulatory element, these
were only found in the population in which PR mapped to LG7, even though
the morphological data indicated large effect QTL for PR in several other
populations as well. Consistent with the available theory and simulations
parameterised on empirical data, we hypothesise that the observed
variability in genetic architecture of PR is due to heterogeneity in the
spatial distribution of standing genetic variation caused by >2x
stronger population structuring among freshwater populations and
>10x stronger genetic isolation by distance in the sea in
nine-spined sticklebacks as compared to three-spined sticklebacks.