Discussion
Inferring the genomic basis of adaptive trait variation, including the
interplay between adaptive divergence and gene flow, remains a central
endeavour in evolutionary biology. To increase rigor, data on both
selective agents and organisms’ multivariate phenotypes are needed when
identifying regions of the genome potentially implicated in adaptation .
We show that there was phenotypic divergence in several traits of
threespine stickleback from Mývatn, Iceland, but little evidence for
genome wide population genomic structure, suggesting extensive gene
flow. However, a combination of GWA and landscape genomics approaches
allowed us to isolate genomic regions associated with both environmental
and phenotypic variation, suggesting genomic divergence in response to
natural selection in face of gene flow.
Phenotypic divergence in the face of
gene
flow
Mývatn stickleback showed spatial divergence in several traits, some of
which was associated with ecological variation. Notably, stickleback
were smaller at the warm shore site, had more armour plates and
relatively longer first dorsal spines in the North than in the South
basin, and relatively longer, but fewer, gill rakers in the rocky shore
site than in the rest of the lake. These results align partially with
previous findings from the same population sampled in 2009 , which found
spatial phenotypic divergence in body size (N basin: larger), spine
length (N basin: longer spines) and gill raker gap width, but no
divergence in lateral plate number. The number of armour plates and
length of spines are important predator defence traits in stickleback ,
with increased predation pressure by birds or fish selecting for more
armour plates and/or longer spines . Mývatn stickleback represent a low
plated morph (range 3 to 10) typical of freshwater environments , but
the higher plate number and longer spines in the N than the S basin
indicates stronger predator induced selection in the N basin. This was
further supported by phenotype-environment association analyses that
showed that Mývatn stickleback had longer second dorsal spines where
piscivorous waterfowl density was higher, and relatively longer pelvic
spines in deeper water. The latter may reflect variation in predation
pressure by altering the occurrence and visibility to visual predators
(e.g., salmonids; ).
Lake fish, including stickleback, often diverge along the
benthic-limnetic axis (reviewed in Wagner & Seehausen 2014), whereby
fish that specialise on a benthic diet have fewer and shorter gill
rakers than those on a limnetic diet . Interestingly, we show that gill
raker divergence (i.e., shorter and more versus longer and less
gill rakers) did not follow a typical benthic-limnetic divergence.
Phenotypic variation in gill raker morphology often reflects diet
mediated trait variation and can facilitate resource polymorphism, from
individual specialization (Bolnick et al. 2003) to spatial
divergence among contrasting environments. Whilst we found some spatial
divergence in gill raker number and length, gill raker morphology was
not associated with any of our environmental measures (including prey
abundances) suggesting that gill rakers may be responding along an
unmeasured axis of divergence. Moreover, our findings contrast to some
extent with who found divergence between Mined and Warm habitats in gill
raker number and gap width rather than gill raker number and length.
This discrepancy might suggest that spatiotemporal variation in
availability of stickleback prey in Mývatn , may induce fluctuating
selection – an interesting target for future research.
Despite observed phenotypic divergence, we found no evidence for
genome-wide divergence, suggesting a single panmictic population and
phenotypic divergence in face-of-gene flow. Although this aligns with
results of , they contrast with those of who found genetic divergence
between two sites and suggested the presence of two morphs ‘Lava’ and
‘Mud’. As above, this discrepancy in genetic divergence may reflect
temporal changes in the extent of spatial genetic divergence and the
loss of previous ecotypes, potentially as a result of strong population
fluctuations in stickleback population size . Notably, population
demographic analyses indicate that the high-density North basin
periodically subsidises the low-density South basin through dispersal ,
which could result in periodic gene flow. However, it is also possible
that differences in the resolution of both spatial sampling and
sequencing may have resulted in the discrepancies between studies.