Evidence of niche divergence
Comparison of ENMs indicated that the S. atlantis, northernS. hesperis , and southern S. hesperis evolutionary
lineages, delineated on the basis of genomic data, significantly differ
in their habitat associations and ecological niches. The relative
magnitude of the “within- vs. between-lineage” coefficient
estimate may be interpreted not only as a measure of the relative
strength of niche divergence, but also as an indicator of whether or not
genomic divergences likely reflect ecological speciation events.
Comparison of these coefficient estimates across models suggest that
niche divergence was greatest between S. atlantis vs. southernS. hesperis , followed by northern S. hesperis vs. southernS. hesperis and S. atlantis vs. northern S.
hesperis , which were approximately equivalent in their strength of
pairwise niche divergence. This ordering corresponds to that of genomic
divergences estimated between S. atlantis and northern and
southern S. hesperis (Fig. 1, Fig. 2, Fig. 3). Although
degree of divergences between pairs of lineages appears to approximately
correspond to degree of geographic separation, null ENMs built from
random localities indicate that observed niche divergences cannot be
attributed to differences in available habitat between lineages
(spurious niche divergence). Furthermore, although northern and southernS. hesperis are largely allopatric in their distributions, our
resistance-based analyses did not detect any significant barriers to
dispersal between them, conferring further support to the hypothesis
that ecologically-based divergent selection has been the principal
process contributing to diversification and reinforcement of the
lineages’ genomic integrity, rather than speciation without selection or
mutation-order speciation associated with barriers to dispersal (i.e.,
vicariance). We therefore suggest that present-day parapatry between
northern and southern S. hesperis is a consequence, rather than
cause, of ecologically-based divergent selection, as projections of
suitable habitat across the entire study landscape demonstrate clear
geographically-structured divergence in habitat associations between the
lineages (Fig. 4).
Assessment of species limits in S. hesperis and S.
atlantis
Our results consistently show that the northern S. hesperislineage is more genetically similar to S. atlantis than to any
genetic clusters within the southern S. hesperis lineage, but we
did not recover any evidence of admixture between S. atlantis and
northern S. hesperis, despite sampling both species in sympatric
portions of their ranges (mostly in Alberta, Canada); these results are
consistent with other genetic surveys (Thompson et al. 2019;
Campbell et al. 2019). Past work has noted differences in
micro-habitat preference between S. atlantis and S.
hesperis in regions where they co-occur (Bird et al. 1995; Guppy
& Shepard 2001; Dunford 2009; Riva et al. 2019), and the results
of our ENMs indicate that divergences in habitat associations are likely
significant enough to limit gene flow between species, even in sympatric
regions. Our results also indicate relatively little mitochondrial and
SNP differentiation between the subspecies S. atlantis hollandi,
S. a. sorocko, and S. a. canadensis relative to the other taxa
in this study. Thus, S. atlantis is an independently
evolving lineage distinct from S. hesperis , and recognition of
the species status of S. atlantis should be maintained.
BFD* species delimitation using SNPs indicated clear support for
splitting northern and southern S. hesperis into distinct species
(Fig. 3a). Both Structure and TESS failed to recover any substructure in
northern S. hesperis despite broad geographic sampling, and
TreeMix and f 3 analyses indicated probable gene flow between
northern S. hesperis, southern S. hesperis, and S.
zerene, particularly in or near the central population of southernS. hesperis (Fig. 2, Table S2). This is also the approximate
boundary between the sampled northern and southern S. hesperislineages, so it is possible that northern S. hesperis expanded
poleward from this geographic region into newly available habitat
following the last glacial retreat, and that these lineages may have
initially continued to exchange genes with each other and S.
zerene . If this hypothesis is accurate, then the lack of recovered
population structure in northern S. hesperis may be partly
reflective of this recent range expansion, as well as due to few
barriers to dispersal and gene flow in the relatively homogenous
prairie/open forest habitat of northern S. hesperis compared to
the more disjunct habitat of southern S. hesperis in the southern
Rocky Mountains. The haplotype sharing between S. zerene and
northern and southern S. hesperis further suggests that
introgression between these species occurred prior to this range
expansion, and emphasizes that COI is only partially informative
for clarifying species boundaries in this complex. ENMs similarly
suggest that ecologically-based divergent selection is likely a
principal process underlying divergence and reinforcement of the
northern and southern lineages, even in the absence of barriers to
dispersal.
Taxonomic revision to S. hesperis
Our results unambiguously support recent evolutionary and ecological
divergences between northern and southern lineages of S.
hesperis , but also indicate that these lineages currently exist as
distinct entities shaped by interactions with other species and the
environment that nonetheless maintain their genomic integrity. We
therefore recommend that the two lineages should be recognized as
distinct species. Following taxonomic priority (Pelham 2019), the
northern lineage should continue to be referred to as S.
hesperis , and the oldest southern subspecies name sampled in this
study, S. h. nausicaa , should be elevated to species level,S. nausicaa , to represent the entire southern lineage. This
taxonomic revision remains a hypothesis that requires further sampling
and genomic assessment, particularly in California and the Great Basin,
where lineages that diverged before the Pleistocene may persist. We also
detected introgression between S. zerene and S. hesperis/S.
nausicaa that may be a source of nuclear gene tree-species tree
discordance. This should be pursued due to the conservation status of
several S. zerene subspecies.