Population structure
Our high-resolution SNP genealogies revealed genetic structure among
marine stickleback from the Atlantic. Specifically, the phylograms based
on SNPs both chosen randomly across the genome and filtered stringently
to reduce the influence of selection consistently recovered three marine
branches (Figure 1c; bootstrap support is given in Figure S1). These
branches were formed by the marine individuals from North Uist and
Ireland (ARDH, OBSM, IR), the two samples from the North Sea (DE, NL),
and stickleback from Canada and Iceland (CA, IS). Within these branches,
however, marine fish from a given location generally did not emerge as
monophyletic, except for the Canadian individuals collected thousands of
kilometers from the nearest sampling locations (IR, IS) (Figure 1b;
overall genome-wide genetic differentiation among the marine samples is
presented in Table S2). In contrast to the marine fish, genetic
structure among our freshwater samples differed fundamentally between
the random and neutral SNP panels (Figure 1c). Based on the former, all
freshwater stickleback together grouped to a single, well-supported
branch distinct from marine fish, and within this freshwater branch,
individuals clustered almost perfectly according to acidic versus basic
habitat. This ecological structure largely vanished when using SNPs
ascertained to reduce the influence of selection. Moreover, contrary to
marine stickleback, freshwater individuals almost consistently grouped
by sampling location, despite the dramatically smaller geographic
distance among the lakes compared to the marine locations (Figure 1b).
All these patterns remained qualitatively consistent when using sparser
data sets, and when replacing individual-level by synthetic genotypes
derived from pooled data (Figure S1). The latter confirms that poolSeq
data enable meaningful genealogical analyses at the population level
(Haenel et al. 2019).
The weak genetic structure among our marine locations within the three
marine branches is consistent with the notion that marine stickleback
display large population sizes, that genetic drift is relatively weak
(Mäkinen et al. 2006; Hohenlohe et al. 2010; Jones et al. 2012a; Catchen
et al. 2013; Roesti et al. 2014; Lescak et al. 2015), and hence that
deleterious genetic variation introduced by hybridization with
freshwater fish should be eliminated efficiently. Nevertheless,
stickleback across the Atlantic clearly do exhibit genetic structure.
Assuming gene flow-selection balance as a cause for the maintenance of
SGV, we would therefore expect differences in the level of SGV among
broad regions within the Atlantic if these regions differed in the input
of maladaptive acidic alleles. A further insight into marine stickleback
is that with both the random and neutral SNPs, the freshwater
populations from North Uist appear genetically no more similar to marine
fish sampled in immediate (ARDH, OBSM) or relative (IR) proximity than
to the samples from the much more distant marine locations. This implies
that at the genome-wide level, any Atlantic marine sample –
irrespective of its precise geographic origin (and including off-shore
samples like IR; Table S1) – serves as an adequate representation of
ancestral Atlantic marine stickleback (see also Kirch et al. 2021).
An intriguing finding emerging from the genealogy is the nearly perfect
segregation of stickleback by habitat when using SNPs sampled at random
across the genome. At first glance, this may stimulate the
interpretation that on North Uist, initially a single freshwater
stickleback form evolved, subsequently differentiated into a single
acidic and basic ecomorph, and these ecomorphs then split into multiple
sub-populations. Apart from being hydrogeographically implausible (see
the Supporting Discussion in Haenel et al. 2019), this interpretation is
challenged by the genetic structure revealed by the neutral SNPs: the
deep separation of freshwater populations on North Uist based on this
marker panel indicates that acidic and basic ecomorphs have arisen
multiple times independently through the adaptive sorting of ancestral
marine SGV (Magalhaes et al. 2016; Haenel et al. 2019; see also Bell et
al. 1993). The contrasting results obtained from random versus neutral
SNPs in freshwater but not marine stickleback highlight, on the one
hand, how deterministically genome-wide polygenic selection and
associated hitchhiking during freshwater adaptation can shape genetic
population structure and thus confound neutral evolutionary history (see
also Berner & Roesti 2017). On the other hand, these results indicate
that the genomes of stickleback populations recently adapted to
ecologically novel freshwater habitats are much more profoundly shaped
by selection than the genomes of the ancestral marine form.