Genomic underpinnings of head and body shape across
lakes:
From our total of 212 SNPs that showed high associations with head
and/or body shape (Figure 2), we found more SNPs associated with body
shape than for head shape. Head shape was controlled by more
large-effect loci relative to body shape and may suggest that head shape
is controlled by fewer genes/pathways. In both cases these will be an
underestimate of actual associations because we have reduced
representation of the genome captured. We found for that for both head
and body shape only a small number of associated SNPs were diverged
between ecomorphs in all four pairs (Figure 3). This is line with what
has been suggested both in other Arctic charr studies and other salmonid
species, in which genetic differentiation between ecomorphs is largely
nonparallel across pairs bar at a few key genes . Further to previous
work, we found that the SNPs shared across pairs were not highly
differentiated between ecomorphs in all pairs suggesting that while
present, they are not critical to underlying the phenotypic differences
in each pair (Figure 4). These results also suggest that the genomic
underpinnings of each phenotype varies across the lakes, likely
contributing to the phenotypic differences we see between pairs. The
polygenic genomic underpinnings of both phenotypes, as indicated by the
numbers of associated SNPs identified, indicate that there are multiple
pathways that can achieve the same phenotypes hence the lack of high
divergence for the same SNPs across all lakes .
Loch Dughaill and in particular Loch Tay often showed notable high
genomic divergence between ecomorphs for many of the associated SNPs for
each trait. Additionally, the associated SNPs for both traits showed
high DXY values compared to the background subsets at
both of these lakes. While increased levels of DXY or
FST compared to genomic background can be indicative of
positive selection , they might also be expected for loci resisting
introgression following secondary contact , as is likely the case in
Loch Tay and Loch Dughaill . The associated SNPs we found are widespread
across the genome (Figure 2) indicating these are not single linked
regions of divergence as found in studies on Atlantic cod and rainbow
trout but instead are diffused and highly polygenic, similar to patterns
for body shape in lake whitefish .
Functional genomic regions for head and body
shape:
Roughly half of the associated SNPs identified for each of head and body
shape were found within or proximal to an annotated gene in the charr
genome. A number of the GO terms that appeared as significantly
overrepresented or enriched in our study have been identified in other
studies investigating adaptive divergences or parallel evolution in
various fish species. Odontogenesis (GO:0042476), sensory perception of
sound (GO:0007605), blood vessel remodelling (GO:0001974), response to
muscle activity (GO:0014850), ventricular trabecula myocardium
morphogenesis (GO:0003222), common-partner SMAD protein phosphorylation
(GO:0007182), cellular response to ethanol (GO:0071361), and
neuromuscular synaptic transmission (GO:0007274) have shown significance
in other Arctic charr studies investigating ecomorph divergence . The GO
terms for associative learning (GO:0008306), regulation of cell shape
(GO:0008360), and UDP-glucuronate biosynthetic process (GO:0006065) also
appear in overrepresented groups in a study on the divergence of a
sympatric lake whitefish species pair (Corgeonus clupeaformis ) in
the USA . Finally, in pupfishes (Cyprinodon. sp. ), the divergent
expression of a number of genes involved in cranial skeletal system
development was seen between different trophic specialists with the GO
term for this process (GO:1904888) significant in our study .
Differences in ossification rate have been related to adaptive
morphological differentiation in other freshwater fish and the over
enrichment or overexpression of genes related to formation of various
bones in our study indicates a similarly important role in adaptive
divergences between ecomorphs of Arctic charr . Indeed, previous work
has noted the importance of differences in bone structure and sizes
between different ecomorphs of Arctic charr .
The QTL database that we have developed allows us to explore whether
rapid replicated diversification of ecomorphs in different salmonid
species is underlined by the use of the same functional regions as has
been previously suggested for salinity tolerance . Our results suggest
that this is true to some extent with QTLs related to body shape in lake
trout and whitefish found in proximity to SNPs that we identified as
being associated with phenotypic differences in Arctic charr ecomorphs.
Whilst we only identified a small number of QTLs located near the
associated SNPs, this is line with other work which suggests that shared
basis for ecomorph divergence across species may be limited . This QTL
marker database will be a valuable resource for future salmonid
research.