1 | INTRODUCTION
Freshwater aquatic organisms in fluvial systems have gene flow
constraints that are associated with the directional flow of water,
habitat heterogeneity and the dendritic nature of the stream network.
Understanding the influences on the evolution of spatial genetic
structure of populations in riverine environments is a unique problem
that involves a specific set of questions, which are described as
riverscape genetics (Davis et al., 2018). Based on the degree of
connectedness of the stream network, the distribution of habitat and
life history of the organism, a directional hierarchy in genetic
diversity of local populations is expected. This is referred to as the
stream hierarchy model (Meffe & Vrijenhoek, 1988). Any modification to
the riverscape structure such as dams, loss of habitat, flooding or
alteration of the drainage system can disrupt the patterns of gene flow
and lead to changes in the expectations of the population genetic
structure (Davis et al., 2018; Meffe & Vrijenhoek, 1988).
The connectivity of stream networks and the species assemblage present
within the upper Mississippi River basin of central North America are
the result of a complex geologic and climatic history. Recurrent,
alternating cycles of glacial advance and retreat by the Laurentide Ice
Sheet during the Quaternary period, 2.6 million to 10,500 years ago,
reshaped and fragmented the regional landscape and altered drainage
patterns and flow regimes (Cupples & Van Arsdale, 2014; Lowe & Walker,
2014; Galloway et al., 2011; Knox, 2007; Figure 1). To the west of the
Mississippi River, the southernmost extent of these glacial advances
occurred during the Pre-Illinoian Glacial Stage (2.6 - 0.3 million years
ago), reaching the present-day Missouri River valley in central Missouri
(Burr & Page, 1986; Hobbs, 1999; Thornbury, 1965; Figure 1). The Ozark
Plateau and associated stream networks to the south of the Missouri
River remained relatively unaffected by the glacial disturbances
(Pflieger, 1975).
The distribution of aquatic species in central North America was notably
affected by the habitat changes in the north, resulting in displacement
or extirpation of local populations (Berendzen et al., 2010; Burr &
Page, 1986). As glacial fronts expanded and retreated the riverscape was
dramatically altered causing changes to the drainage pattern, flow
regime and habitat (Thornbury, 1965). West of the Mississippi River, the
Ozark Plateau provided a refugium for many fish species during the
periodic glacial advances of the Quaternary period (Berendzen et al.,
2003; Berendzen et al., 2010; Burr & Page, 1986; Echelle et al., 2014;
Near et al., 2001). Following the retreat of the last glacial maximum
(19,000 to 10,500 years ago), new dispersal opportunities were created
among the newly formed stream connections, which contributed to the
expansion of populations northward and the establishment of the
contemporary fish assemblage (Berendzen et al., 2010; Burr & Page,
1986; Ray et al., 2006).
Etheostoma caeruleum , the rainbow darter, is a member of this
assemblage with a broad distribution in small rivers, creeks, and
streams in the Mississippi River drainage across eastern North America
(Ray et al., 2006; Strange & Burr, 1997; Figure 2). The species is a
small, sexually dimorphic fish that displays a preference for shallow,
fast-flowing water within gravel or rubble riffles (Harding et al.,
1998; Mueller et al., 2020). Mature individuals exhibit high
site-fidelity to their natal habitats throughout their life cycle, with
breeding males migrating up to 1 km during spring spawning periods
(Hicks & Servos, 2017). The rainbow darter is a benthic invertivore
that actively forages for a variety of macroinvertebrates that inhabit
riffles. Their preferred food sources are much less abundant in the
deeper pools separating riffle structures (Mueller et al., 2020). In
addition, E. caeruleum is considered a sentinel species and is
relatively sensitive to habitat and water quality changes due to channel
siltation, chemical runoff, and related effects of anthropogenic
activity (Haponski et al., 2009; Tonnis, 2006).
West of the Mississippi River, E. caeruleum has a disjunct
distribution inhabiting streams in the upper Mississippi River basin and
the Ozark Plateau, but is absent in the intervening region (Figure 2).
In tributaries of the upper Mississippi River, local populations of the
rainbow darter have a patchy, disjunct distribution across the
riverscape (Davis et al., 2015). Areas of local concentration are often
separated by large river distances. This pattern results from the direct
impact of glacial processes on the landscape causing the spatial
distribution of suitable habitat to be highly fragmented and
heterogeneous. Modern river drainages in this region, flow through
varying depths of glacial drift overlaying the Tertiary bedrock
topography (Burr & Page, 1986; Thornbury, 1965). In contrast, the
drainage patterns of the Ozark Plateau have maintained their basic
configuration since the late Paleozoic era (Pflieger, 1975). Modern
river drainages in this region are characterized by clear, cool high
gradient streams with course substrate in deeply dissected valleys
(Pflieger, 1975; Thornbury, 1965). Local populations of the rainbow
darter in this region are widespread and nearly continuous, resulting
from the abundant distribution of suitable habitat. The rainbow darter
is one of the most abundant fish species in the Ozarks (Pflieger, 1975).
In this study we compare the fine-scale population genetic structure of
rainbow darter populations in two similar river systems, one located in
the glaciated environment of the upper Mississippi River basin and one
in the unglaciated environment of the Ozark Plateau. We test the
hypothesis that climatic and geologic processes during the Quaternary
period influenced the observed genetic signature and disrupted
expectations under riverscape genetic models. Under the stream hierarchy
model, the population genetic structure is consistent with the structure
of the stream network, distance between local populations, connectedness
of the habitat and life history of the organism (Brauer et al., 2018;
Meffe & Vrijenhoek, 1988). Since the rainbow darter exhibits high site
fidelity and short dispersal distances, the expectation is that local
populations will be partially isolated with limited geneflow and
evidence of isolation by distance in an upstream to downstream pattern.
We predict that the population genetic structure of E. caeruleumin the glaciated environment in the North will not fit expectations
under the stream hierarchy model and will exhibit low levels of genetic
diversity. Conversely, we predict that the population genetic structure
of E. caeruleum in the unglaciated environment in the South will
fit expectations under the stream hierarchy model and exhibit higher
levels of genetic diversity. In this study, we utilize genome-wide SNPs
generated using RADseq to infer fine-scale population genetic structure
in each river system.