ORIGINAL RESEARCH

published: 17 January 2022

doi: 10.3389/fevo.2021.790829

The Role of Directed Dispersal in

Driving Genetic and Morphological
Structure in Invasive Smallmouth
Bass
Genevieve Diedericks 1,2* , Chris Broeckhoven 3 , Sophie von der Heyden 2 , Olaf L. F. Weyl 4†
and Cang Hui 5,6
1
Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa,
2
Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa,
3
Department of Biology, Laboratory of Functional Morphology, University of Antwerp, Antwerp, Belgium, 4 Centre
for Invasion Biology, South African Institute for Aquatic Biodiversity, Makhanda, South Africa, 5 Centre for Invasion Biology,
Department of Mathematical Sciences, Stellenbosch University, Stellenbosch, South Africa, 6 Mathematical Biosciences
Group, African Institute for Mathematical Sciences, Cape Town, South Africa

Dispersal is an essential life-history trait crucial to species persistence and diversification.

This is particularly important in spatiotemporal fluctuating environments such as
Edited by:
freshwater habitats, where species movement is confined to the dendritic network and
Shannon J. McCauley,
University of Toronto Mississauga, wetted boundaries. To persist in such fluctuating environments, a species can modify,
Canada adaptively and plastically, its phenotypic variation to better match the environment
Reviewed by: or escape via directed dispersal to a more suitable habitat (i.e., matching habitat
Erika Rubenson,
Four Peaks Environmental Science &
choice). We use the invasive smallmouth bass, Micropterus dolomieu, sampled at
Data Solutions, United States 10 km intervals, to assess the effect of directed dispersal on the fine scale genetic and
Liz Alter,
phenotypic variation in populations of M. dolomieu along a river course. Gene flow was
California State University, Monterey
Bay, United States used as a proxy for dispersal. By comparing population genetic structure, morphological
*Correspondence: variation (of linear traits and geometric landmarks), and environmental heterogeneity,
Genevieve Diedericks we discovered a clear correlation between environmental variation and morphological
[email protected]
† Deceased
traits. Although isolation by distance seemed to have shaped the overall genetic pattern
detected among the populations, the strong genetic structuring observed within the
Specialty section: Ratel tributary appeared to be non-random. These results provide novel insights into the
This article was submitted to potential mechanisms promoting the spread and establishment of invasive species and
Behavioral and Evolutionary Ecology,
a section of the journal the possible influence multiple introductions may have on fine scale genetic structuring.
Frontiers in Ecology and Evolution
Keywords: freshwater fish, matching habitat choice, ecomorphology, Wahlund effect, gene flow, genetic diversity
Received: 07 October 2021
Accepted: 30 November 2021
Published: 17 January 2022
INTRODUCTION
Citation:
Diedericks G, Broeckhoven C, Dispersal is a life-history trait essential to the persistence, diversification and evolution of species
von der Heyden S, Weyl OLF and (Edelaar and Bolnick, 2012; Saastamoinen et al., 2018). Although exchange of individuals between
Hui C (2022) The Role of Directed
populations has typically been considered to occur at random (Patterson et al., 2008; Clobert et al.,
Dispersal in Driving Genetic
and Morphological Structure
2009), a paradigm shift is changing the way dispersal is perceived. No longer thought to occur
in Invasive Smallmouth Bass. at random, active dispersal can reflect the response of individual phenotypes to the surrounding
Front. Ecol. Evol. 9:790829. environment (Bowler and Benton, 2005; Edelaar et al., 2008; Clobert et al., 2009; Edelaar and
doi: 10.3389/fevo.2021.790829 Bolnick, 2012; Hui et al., 2012; Jacob et al., 2015). As many environments are known to be both

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Diedericks et al. Directed Dispersal in Smallmouth Bass

spatially heterogeneous and temporally variable (Bonte and Langerhans, 2008; Langerhans and Reznick, 2010). Indeed,
Dahirel, 2017), individuals need to sample and compare different Drakou et al. (2009) demonstrated that dispersal limitations
environments while making decisions on their next move play a bigger role in structuring fish communities than
(Edelaar et al., 2008; Zhang and Hui, 2014). Dispersing away habitat heterogeneity.
from core populations not only benefits individuals with reduced Within freshwater ecosystems, invasive fish have been
competition intensity (Dytham, 2009; Rubenson and Olden, particularly favored as model organisms due to their superior
2017) but may also provide opportunistic niches and resources dispersal abilities, essential for invasion success, when compared
for survival (Ronce, 2007; Clobert et al., 2009). to native fishes (Lodge et al., 1998; Sala et al., 2000; Beisel,
As a phenotype-environment mismatch is bound to occur 2001; Rubenson and Olden, 2017). Moreover, it has been shown
in any heterogeneous environment, species could mitigate the that dispersal opportunities, rather than species composition or
mismatch by fine-tuning its phenotypic variation or simply favorable abiotic conditions of the recipient community, are
preserving a general-purpose phenotype via phenotypic plasticity an important component mediating aquatic invasions (Ricciardi
or local adaptation (Richards et al., 2006). Individuals can also and MacIsaac, 2000). This is likely because introduced fish are
move into more suitable environments via matching habitat often from mixed genetic stock (Diedericks et al., 2018a,b), and
choice (Edelaar et al., 2008; Edelaar and Bolnick, 2012; Camacho unlikely to exhibit fine genetic structuring or matching habitat
and Hendry, 2020). Matching habitat choice, as proposed by choice, as one would expect for native fish.
Edelaar et al. (2008) states that individuals will select and One such freshwater invader is the smallmouth bass,
settle in environments that complement their phenotype, and Micropterus dolomieu. Native to the east-central parts of
in doing so drive directed dispersal. All three mechanisms the United States of America and two Canadian provinces,
can jointly affect local performance, population structure and M. dolomieu is currently recognized as an invasive species
genetic diversity (Arendt, 2015; Nicolaus and Edelaar, 2018). For in at least 12 countries worldwide, including South Africa
instance, increasing the rate of random dispersal can genetically (Loppnow et al., 2013). Although M. dolomieu has been
homogenize populations, by reducing genetic differentiation described as a sedentary species when inhabiting riverine
between populations (Haldane, 1948; Endler, 1973; Slatkin, 1985) environments, establishing and guarding home ranges (Todd and
and potentially limiting local adaptation (Edelaar and Bolnick, Rabeni, 1989; Ridgway and Shuter, 1996), studies have observed
2012; Jacob et al., 2015) and even speciation (Lucek et al., remarkable fluctuations in dispersal behaviors when populations
2013). In contrast, directed dispersal (associated with matching are subjected to environments with fluctuating habitat suitability,
habitat choice) is thought to promote genetic differentiation and often leading to extensive movement in an attempt to colonize
potentially local adaptation when coupled with natural selection new habitats (Lyons and Kanehl, 2002; Hui and Richardson, 2017;
(Benkman, 2016), ultimately increasing local population genetic Rubenson and Olden, 2017). Moreover, in a recent study by
structure (Edelaar et al., 2008; Edelaar and Bolnick, 2012). Indeed, Diedericks et al. (2018a), significant population genetic structure
in a recent simulation study by Nicolaus and Edelaar (2018), was detected for M. dolomieu across the invaded South African
incorporating both neutral and functional traits in addition to range. However, little is known about the species’ genetic diversity
mild environmental fluctuations, the authors observed random and phenotypic variability at fine spatial scales, both essential
dispersal to erode population genetic structuring, while non- components to the successful establishment and spread of an
random dispersal maintained strong population differentiation invasive species (Prentis et al., 2008).
with little within-population variance. However, despite directed Considering the aforementioned, we investigate the fine scale
dispersal receiving increased attention, few empirical studies genetic- and phenotypic variation in populations of M. dolomieu
have sought to test matching habitat choice (Benkman, 2016; within an invaded river system in South Africa. Following the
Camacho et al., 2020), especially for introduced species in matching habitat choice hypothesis, we predict: (1) M. dolomieu
their invaded ranges. to display strong genetic population structuring with little
Lotic systems in hydrologically diverse regions are within-population variance; and (2) a strong correlation between
characterized by extensive spatiotemporal fluctuations in phenotype and environment along the river course. In contrast,
both biotic and abiotic conditions (Winemiller et al., 2010). should dispersal occur at random, we would expect homogenous
Thus, fish that inhabit such environments are expected to genetic population structure across sampled populations and
match their environment and adapt swiftly to these pressures by no phenotype-environment correlation. Understanding the
maximizing their locomotive capabilities essential for feeding, interplay between morphology, genetics and the environment
spawning and predator avoidance (Via et al., 1995), which and how species movement may affect it, is of fundamental
may be of particular importance in the face of climate change importance when considering future range expansions of
and anthropogenic activities. Nevertheless, most freshwater invasive species.
fishes often face movement constraints, as dispersal is limited
to the wetted boundaries, and in riverine environments, the
dendritic network (Garant et al., 2007; Olden et al., 2010). In MATERIALS AND METHODS
this regard, numerous studies on freshwater fishes have revealed
the correlation between functional traits and environmental Study System and Sampling
variations (e.g., swimming and feeding performance; Keast The Olifants River is one of the largest river systems within
and Webb, 1966; Vogel, 1994; Langerhans et al., 2003; the Western Cape (WC) Province of South Africa, with an

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Diedericks et al. Directed Dispersal in Smallmouth Bass

approximate length of 285 km and a catchment area of sub-catchment – “RS,” (3) flow length (i.e., the number of
46,220 km2 . The WC has a Mediterranean climate, with the upstream stream grid cells) – “FL” and (4) flow accumulation
Olifants River catchment receiving ∼ 90% of its rainfall in (i.e., the total number of upstream grid cells) – “FA.”
the winter months (Soderberg, 2003). In addition, the rain Second, four variables that classify the soil type were obtained,
shadow effect sees the Cederberg Mountains to the East of including (5) sand content mass fraction across sub-catchment –
the Olifants River receive double the amount of rain when “SNDPPT,” (6) silt content mass fraction across sub-catchment –
compared to the main river valley (Soderberg, 2003; Figure 1). “SLTPPT,” (7) clay content mass fraction across sub-catchment –
Extensive agricultural development and farming activities has “CLYPPT” and (8) coarse fragments (>2 mm fraction)
occurred within the valley, leading to an increase in alien volumetric across sub-catchment – “CFRVOL.” Lastly, we
invasive vegetation and sedimentation, modified river bed, and extracted eight bioclimatic variables, four characterizing air
reduced water quality (DWA, 2006; Supplementary Figure 1). temperature and four describing precipitation averaged across
Moreover, due to large amounts of water being used for sub-catchment, which were derived from the WorldClim
irrigation in the middle reaches of the Olifants, large stretches database (Hijmans et al., 2005). Bioclimatic variables comprised
of the main stem often dry up entirely during the summer (9) annual mean temperature – “BIO1,” (10) maximum
months (DWA, 2006; Supplementary Figure 1). Despite the temperature of warmest month – “BIO5, (11) temperature
dire state of the Olifants River main stem, the tributaries annual range – “BIO7,” (12) mean temperature of warmest
and upper reaches still harbor near-pristine ecosystems (DWA, quarter – “BIO10,” (13) annual precipitation – “BIO12,” (14)
2006). Two mainstream impoundments, namely Bulshoek and precipitation of wettest month – “BIO13,” (15) precipitation
Clanwilliam Dam, constructed in 1919 and 1935, respectively, seasonality (i.e., coefficient of variation) – “BIO15” and
are situated within the Olifants River (Figure 1). Clanwilliam (16) precipitation of wettest quarter – “BIO16” (Domisch
Dam possesses sluice gates and as such, prohibits upstream et al., 2015). As Domisch et al. (2015) showed a strong
fish movement. Micropterus dolomieu, initially introduced for correlation between water- and air temperature, the latter was
recreational fishing purposes, was released into the upper reaches used as a proxy for water temperature. Due to the highly
of the Olifants River system in 1943 and 1945 (from the correlated nature of the environmental variables, a principal
same breeding stock) and has since successfully invaded and component analysis (PCA) was conducted to avoid potential
established itself throughout the Olifants River system and its problems associated with multicollinearity. The PCA reduced
tributaries, including the two impoundments (Van der Walt et al., the dataset to a smaller number of independent PC scores
2016). Although only one introduction event was historically (hereafter referred to as “PCENVIRONMENT ”), which were used in
recorded for M. dolomieu, Diedericks et al. (2018a) propose that subsequent analyses.
multiple introductions offer a more likely scenario.
Approximately 20 M. dolomieu specimens were collected from Morphometric Measurements
ten localities spanning ∼100 km (total sample size, n = 203) in the Both linear and geometric measurements of morphometrics
austral summer (January – March) of 2015. Sampling occurred at were employed to test for a correlation between phenotype
approximately 10 km intervals and encompassed two tributaries, and environment. All measurements were taken on fresh,
the Jan Dissels River (localities A-C) and the Ratel River (locality unpreserved specimens. Firstly, a standardized photograph of
J) as well as the main stem of the Olifants River, including the left lateral side of each fish was taken with a digital
the Clanwilliam Dam (localities D-I; Figure 1). All specimens Sony DSC-HX100V camera. To ensure standardized images,
were collected by angling (CapeNature permit number: 0056- the unpreserved specimens were pinned to laminated graph
AAA043-00004) using standardized lure sizes, before being paper and a tripod, set to a standard height, was used. To
euthanized with clove oil (Ethical clearance reference number quantify and visualize the body shape change between localities,
SU-ACUM14-00011, Stellenbosch University). A piece of muscle 12 unambiguous and homologous landmarks were digitized
tissue was excised from the abdomen and stored in 70% ethanol using tpsDig2 version 2.17 software (Rohlf, 2013; Figure 2 and
for DNA extraction. Supplementary Data Sheet 1). Twenty-five linear morphological
characters, representing both swimming and feeding traits
Environmental Data (Winemiller, 1991; Table 1, Figure 2, and Supplementary Data
Data characterizing the river topology, soil classification and Sheet 1), were measured on site using digital calipers (model
hydroclimate for the Olifants River system were obtained from IP67, Mitutoyo Ltd., Japan) with a precision of 0.01 mm. In
a near-global data set consisting of freshwater environmental addition, an otolith from each fish was removed, cleaned and
variables (in a standardized 1 km grid) derived by Domisch et al. stored for aging analysis. Following the procedure described by
(2015). Given the potentially large spatial and temporal variation Taylor and Weyl (2013), each otolith was sectioned and the
(Soderberg, 2003), and consequently large measurement error, growth rings counted to determine the age of each specimen. To
localized environmental variables (e.g., pH, dissolved oxygen, ensure accurate age estimation, the specimens were aged by two
salinity, etc.) were omitted. For each sampling locality, 16 of the authors (GD and OW) independently.
variables (Supplementary Data Sheet 1) were extracted using A PCA conducted on all the linear morphometrics revealed
the R packages RASTER 2.5-8 (Hijmans, 2016) and SP 1.2- one axis, coined “body size,” which explained 92.8% of the
4 (Pebesma, 2016). Firstly, four variables related to river total variation (Eigenvalue = 23.2). To correct for size variation
topography were calculated. These include (1) average elevation among populations, each linear morphometric variable was
across sub-catchment – “ELE,” (2) average river slope across regressed against body size. The resulting residuals were kept

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Diedericks et al. Directed Dispersal in Smallmouth Bass

FIGURE 1 | The sampling localities within the Olifants River system of the Western Cape, South Africa. All letters (A – J) represent sampled localities used for the
linear and geometric morphometric measures, while localities sampled for the genetic analyses are indicated with an asterisk (*). Localities A – C represent those
sampled in the Jan Dissels River tributary, while locality D represents the Clanwilliam Dam. Localities E – I represent sampled localities situated within the mainstem
of the Olifants River and locality J represents the Ratel River tributary. The Clanwilliam Dam sluice gates are indicated with an arrow.

for further analyses. Subsequently, a PCA was conducted each of the landmark coordinates. These residuals were
on these residuals, retaining the most significant PC axes then used to construct a covariance matrix, before a PCA
(hereafter referred to as “PCLINEAR ”). The PCLINEAR axes were was performed to reduce the dimensionality of the data
also compared between the localities using univariate F-tests, (hereafter referred to as “PCSHAPE ”). Furthermore, univariate
with age as covariate and the interaction effect of age∗ locality F-tests were employed to compare the PCSHAPE axes between
included. Bonferroni post hoc analyses were conducted to identify localities, with age and the interaction effect of age∗ locality
differences between localities. included as covariates. Successive Bonferroni post hoc tests
To analyze the geometric landmark coordinates representing were conducted to determine differences in body shape
body shape variation, MorphoJ (Klingenberg, 2011) was between localities.
employed. Firstly, a Procrustes superimposition was performed A generalized linear model was used to test for the effects of
on the “raw” coordinates to remove orientation, size and environment on morphology, with PCLINEAR and PCSHAPE scores
position biases from the data (Klingenberg, 2011). The as dependent variables and PCENVIRONMENT as independent
resulting Procrustes coordinates were regressed against variables. Statistical analyses were conducted in SPSS STATISTICS
centroid size (CS) to obtain size corrected residuals for v. 20.0.0 (SPSS Inc., Chicago, IL, United States).

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Diedericks et al. Directed Dispersal in Smallmouth Bass

FIGURE 2 | The 12 geometric morphometric landmark positions ( ) and 21 of the 25 linear morphometric measurements taken for each specimen. The four linear
measurements associated with the mouth (mouth height – MoH, mouth width – MoW, Length of snout with mouth open – LSO and Length of snout with mouth
closed – LSC, are not illustrated. Linear morphometric measurement numbers correspond to those in Table 1.

TABLE 1 | Mean and standard deviation for each of the linear morphometric measurements.

Trait# Morphological characters Abbrev. Mean ± SD (cm) Trait # Morphological characters Abbrev. Mean ± SD (cm)

1 Standard body length SBL 20.36 ± 7.47 14 Dorsal fin height DFH 30.02 ± 12.37
2 Maximum body height MBH 50.97 ± 21.75 15 Caudal fin length CFL 41.62 ± 13.66
3 Maximum body width MBW 26.34 ± 11.34 16 Caudal fin height CFH 69.84 ± 27.59
4 Caudal peduncle length CPdL 9.80 ± 3.12 17 Anal fin length AFL 27.15 ± 10.42
5 Caudal peduncle height CPdH 25.92 ± 16.95 18 Anal fin height AFH 24.59 ± 9.21
6 Caudal peduncle width CPdW 6.50 ± 1.80 19 Pectoral fin length PtFL 31.27 ± 22.93
7 Head length HL 45.64 ± 15.58 20 Pectoral fin height PtFH 14.47 ± 6.85
8 Head height HH 41.67 ± 18.30 21 Pelvic fin length PFL 24.26 ± 8.09
9 Head width HW 25.85 ± 10.51 22 Pelvic fin height PFH 16.73 ± 6.31
10 Eye height EH 11.56 ± 2.52 23 Length of snout with mouth closed LSC 19.38 ± 7.44
11 Mouth height MoH 32.02 ± 10.13 24 Length of snout with mouth open LSO 24.89 ± 9.27
12 Mouth width MoW 34.08 ± 11.37 25 Body midpoint height BMH 29.74 ± 11.75
13 Dorsal fin length DFL 39.33 ± 16.02

The corresponding trait number and abbreviation (Abbrev) correspond to those used in text and in Figure 2.

Genetic Analyses subunit I (COI) and cytochrome b (cytb)] were sequenced.

For the genetic analyses, seven of the ten localities were included PCR reactions and cycling conditions followed those in
(n = 139) and encompassed the four populations in the two Diedericks et al. (2018b).
tributaries (localities A-C: Jan Dissels River; locality J: Ratel To characterize genetic variation, population structure
River), Clanwilliam Dam (locality D), and two main stem and gene flow among the sampled populations, individuals
populations (localities H – I; Figure 1). Total genomic DNA was were genotyped using nine nuclear microsatellite markers
extracted from M. dolomieu muscle tissue using the NucleoSpin (Mdo3, Mdo4, Mdo5, Mdo7, Mdo8, Mdo9, Mdo10, Mdo11,
Tissue extraction kit (MACHEREY-NAGEL, Separations, Cape Lma21; Colbourne et al., 1996; Malloy et al., 2000). Three
Town, South Africa) following the manufacturers protocol. All multiplex reactions were used to amplify the loci and
DNA extractions were kept at −20◦ C. To confirm that the followed the protocol described in Diedericks et al. (2018a,b);
collected individuals do not include hybrids of smallmouth Supplementary Data Sheet 1. Microsatellites were genotyped
x largemouth bass (see Diedericks et al., 2018b), two partial on an automated sequencer (ABI 3730 XL DNA Analyzer,
mitochondrial (mtDNA) gene regions [cytochrome oxidase Applied Biosystems, CAF, Stellenbosch, South Africa) before

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Diedericks et al. Directed Dispersal in Smallmouth Bass

being visually inspected, aligned and scored in Geneious 10.0.2

R
(b) to prevent failure to detect fine scale genetic structure.
(Biomatters, Auckland, New Zealand). Bootstrap re-sampling (10,000) was run to calculate the 95%
To evaluate the dataset for amplification errors associated confidence interval.
with stuttering and large allele drop-out, Microchecker 2.2.3
(Van Oosterhout et al., 2006) was used. Genepop 4.2.1 Connectivity and Dispersal
(Rousset, 2008), employing the Bonferroni method to correct for To test for isolation by distance (IBD) among populations,
multiple comparisons (Rice, 1989), was used to assess all loci a Mantel test (Mantel, 1967) was conducted in GenAlEx 6.5.
for deviations from Hardy-Weinberg equilibrium (HWE) and Significance was assessed using 10,000 permutations. Assignment
linkage disequilibrium. As most of the populations deviated from tests have great power when wanting to detect migrants using
HWE, the EM algorithm (Dempster et al., 1977) implemented multilocus genotypes (Manel et al., 2005). As such, two Bayesian
in FreeNA 1.2 (Chapuis and Estoup, 2007), was utilized to approaches, both implemented in Geneclass 2.0 (Piry et al.,
check for the presence of null alleles. Nuclear genomic variability 2004), were used to estimate connectivity and migration between
within sampled populations was assessed as allelic richness (AR), sampled populations. Geneclass uses both genetic distance and
number of alleles (Na), observed heterozygosity (HO ), expected allele frequencies, in conjunction with a MCMC resampling
heterozygosity (HE ), and Wright’s inbreeding coefficient (FIS ), algorithm, to identify migrants (Piry et al., 2004; Putman and
calculated in FSTAT 2.9.3.2 (Goudet, 1995), Genepop 4.2.1 and Carbone, 2014). Firstly, an assignment test (Cornuet et al., 1999),
Arlequin 3.5.2.2 (Excoffier and Lischer, 2010). The statistical using the Bayesian criterion of Rannala and Mountain (1997),
significance of FIS was determined after 1,000 permutations was conducted to determine whether all specimens originated
in FSTAT 2.9.3.2. from the localities in which they were sampled. This was done
Genetic population structure was investigated using a by comparing each individuals’ genotype to a simulated dataset.
five-pronged approach. Firstly, FSTAT 2.9.3.2 was used The simulation algorithm by Paetkau et al. (2004) was selected,
to calculate FST to assess genetic differentiation between as this method has been shown to accurately detect dispersing
sampled localities. Statistical significance was calculated using individuals even when all potential source populations were not
a Bonferroni correction. Secondly, an analysis of molecular sampled (Cornuet et al., 1999; Paetkau et al., 2004). The Type
variance (AMOVA), implemented in Arlequin 3.5.2.2 and I error was set to 0.01 and 10,000 individuals were simulated.
statistical significance ascertained using 10,000 permutations, Secondly, to assess the dispersal of M. dolomieu within the
was conducted to reveal the extent of population subdivision Olifants River system, we used the “detect migrant” function in
among sampled populations. Thirdly, using allele frequencies Geneclass 2.0 with the Bayesian criterion defined by Rannala
we explored the genetic associations within and among the and Mountain (1997). This method explicitly seeks and identifies
sampled localities with a PCA, conducted in the R package first generation (“direct”) migrants (Paetkau et al., 2004; Piry
Adegenet 1.3.1 (Jombart and Ahmed, 2011). Fourthly, the et al., 2004), i.e., individuals originating from a population other
Bayesian clustering approach, as implemented in STRUCTURE than the one they were sampled from. As not all potential
2.3.4 (Pritchard et al., 2000), was used to identify and visualize source populations may have been sampled, we selected the
the spatial population structuring along the river. Simulations L_home/L_max likelihood computation method (Paetkau et al.,
employing the admixture model and assuming correlated allele 2004). The simulation algorithm (Paetkau et al., 2004), number of
frequencies, were run five times for each K (1 < K < 10). The simulations (10,000) and the type I error (0.01) mimicked those
initial burn-in was set to 70,000 Markov Chain Monte Carlo used in the assignment test.
(MCMC) generations, followed by 300,000 MCMC iterations. Lastly, to ascertain the effect of genetic variation and dispersal
The results were collated and the most probable K determined on the morphology-environment relationship, four canonical
using the Evanno method (Evanno et al., 2005), as implemented correspondence analyses (CCA) were run. All analyses were
in Structure Harvester 0.6.94 (Earl, 2012). Finally, Clumpp 1.1.2 conducted at the individual level and comprised the residual
(Jakobsson and Rosenberg, 2007) and Distruct 1.1 (Rosenberg, linear morphometric values. Due to the correlated nature of the
2004) were used to generate and visualize the final results. environmental variables, five variables were chosen to represent
Lastly, as the underlying STRUCTURE model assumes HWE the river topology, soil classification and hydroclimate; annual
and, according to the STRUCTURE manual, may not be suited mean temperature – BIO1, annual precipitation – BIO12, average
to spatially distributed data with localized dispersal (Pritchard river slope – RS, flow accumulation – FA, coarse fragments
et al., 2010), we tested for spatial autocorrelation within our volumetric across sub-catchment – CFRVOL. The first CCA
dataset, as suggested by Schwartz and McKelvey (2009). Spatial was used to explore the correlation between the morphological
autocorrelation (r) investigates the spatial genetic structure traits and the environmental variables (Supplementary Data
among sampled individuals, using pairwise genetic distances Sheet 1). The second, third and fourth analyses, all partial CCA’s,
over a given geographic distance (i.e., watercourse distance, investigated the same morphology-environment relationship,
km) (Smouse and Peakall, 1999). GenAlEx 6.5 (Peakall and but considered the additional influence of genetic variation,
Smouse, 2006) was used to assess the spatial autocorrelation dispersal and a combination of genetic variation and dispersal,
among sampled individuals, analyzing the data at two different respectively (Supplementary Data Sheet 1). Individual allele
distance classes, i.e., (a) five classes of 20 km and (b) 10 classes frequencies were used to represent the genetic variation, while the
of 10 km, with 9,999 permutations. This was done (a) to probabilities associated with the assignment test (i.e., probability
ensure large enough sample sizes for statistical power and of an individual originating from the sampled locality versus

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Diedericks et al. Directed Dispersal in Smallmouth Bass

other localities) were used as a proxy for dispersal. Analyses were The PCA of the 16 environmental variables retained two
conducted using the “vegan” R package (Dixon, 2003), while PC axes which explained 94.8% of the total variation. The
the significance of these associations was calculated using the first PC axis, PCENVIRONMENT 1 , was negatively correlated
anova.cca function (Dixon, 2003) with 999 permutations. with elevation, slope, percentage of coarse fragments and
temperature, but positively correlated with flow length, flow
accumulation, precipitation and clay content (Supplementary
RESULTS Table 3). Therefore, PCENVIRONMENT 1 represents a gradient from
fast-flowing streams at high altitude to wide, slow-flowing rivers
Fish Morphology at lower altitude. PCENVIRONMENT 2 was positively correlated
Significant variation in size (ANOVA; F 9 ,191 = 38.37, P < 0.001) with percentage of sand, as well as air temperature across
and age (ANOVA; F 9 ,191 = 14.03, P < 0.001) was observed among the sub-catchment, but negatively correlated with elevation
localities. Specimens collected at locality D were approximately and silt content (Supplementary Table 3). Environment
twice the size of specimens from other localities (Bonferroni (PCENVIRONMENT 1 ) had a significant effect on body depth
post hoc tests, all P < 0.001). Size variation was rather limited (PCLINEAR 1 ; standardized β = 0.77; P = 0.01) and gape size
after excluding specimens from locality D (15.1 – 21.8 cm (PCLINEAR 2 ; standardized β = −0.75; P = 0.01) (Figure 4)
SBL). Fish belonging to locality A and D were significantly but not on the remaining size (PCLINEAR 3−9 ; standardized
older (Bonferroni post hoc tests, all P ≤ 0.03) than those β = −0.28 – 0.35; all P ≥ 0.32) or shape measurements
of the other localities (Supplementary Figure 2), although (PCSHAPE 1−4 ; standardized β = −0.26 – 0.46, all P ≥ 0.10). In
no significant difference in age was observed among the contrast, PCENVIRONMENT 2 had no effect on size (PCLINEAR 1−9 ;
other populations. standardized β = −0.28 – 0.54; P ≥ 0.11) and shape (PCSHAPE
The PCA conducted on the Procrustes coordinates provided 1−4 ; standardized β = −0.45 – 0.07; P ≥ 0.19) measurements.
four PCSHAPE axes (eigenvalues PCSHAPE 1 = 4.90; PCSHAPE
2 = 1.64, PCSHAPE 3 = 1.41, PCSHAPE 4 = 1.21), jointly
explaining 67% of the variation, which were retained for the Genetic Diversity and Population
geometric morphometric data analyses. Shape PC1 (PCSHAPE Structure
1 ) corresponds to a dorsal to ventral redistribution in body A total of 139 specimens, collected from seven localities, were
shape, while PCSHAPE 2 corresponds to rounded bodies in successfully sequenced (for cytb and COI) and genotyped at
addition to shortened caudal peduncles (Figure 3). Similarly, nine microsatellite loci. When comparing these sequences to
PCSHAPE 3 represented fish with wider bodies, while PCSHAPE the Diedericks et al. (2018b) alignment and NCBI BLAST
4 denoted slender fish with large heads and shortened caudal results, no hybrid or introgressed individuals were obtained;
peduncles (Supplementary Figure 3). The univariate F-tests hence all 139 specimens were used in subsequent analyses. No
revealed significant differences in PCSHAPE 1 , 2 , 4 among amplification errors (i.e., stuttering, large allele drop-out), linkage
localities, although a statistically significant interaction effect disequilibrium or null alleles were detected in the microsatellite
age∗ locality was present in PCSHAPE 2−3 (Supplementary dataset. The majority of loci and populations did, however,
Table 1). Bonferroni post hoc tests indicated that fish from locality not conform to Hardy-Weinberg expectations, likely due to the
A had higher bodies (PCSHAPE 1 ) than the other populations, with significant heterozygote deficit associated with the high levels of
only marginal variation being observed with regards to locality B inbreeding (FIS ; Table 2). Observed heterozygosity (HO ) ranged
and D (Figure 3). from 0.150 (locality D) to 0.950 (locality H) across all loci, while
The PCA of the 25 linear morphometric measurements the expected heterozygosity (HE ) ranged from 0.152 (locality A)
retained nine PC axes (PCLINEAR 1−9 ; Supplementary Table 2). to 0.756 (locality D). Marginally higher allelic richness values,
Principal component 1 (PCLINEAR 1 ) represented fish with based on a minimum of 15 specimens, was observed for the two
higher bodies (MBH), higher and narrower caudal peduncles mainstem localities (locality H and I) and the Ratel tributary
(CPdH and CPdW, respectively), an increased head height (HH), (locality J; Table 2).
and decreased eye height (EH), anal fin height (AFH) and Pairwise FST values revealed varying levels of differentiation
pelvic fin length (PFL). Hence, PCLINEAR 1 represents fish with (FST = 0.0269 – 0.4320) between localities, with all but two
“deeper bodies” (Figure 3). Principal component 2 (PCLINEAR 2 ) comparisons statistically significant after Bonferroni correction
corresponded to “gape size,” as the highest loading scores were (Supplementary Table 4). The AMOVA results assigned
related to mouth height and width (MoH, MoW; Supplementary the largest amount of genetic variation to within each
Table 2). The univariate F-tests revealed differences in all locality (78.98%), with limited variation being observed among
PC axes among localities except PCLINEAR 9 (Supplementary tributaries (14.64%) or among localities within tributaries
Table 1). Bonferroni post hoc tests further revealed that locality (6.38%). All three variance components were statistically
A had less deep bodies when compared to the other localities significant (P < 0.001). The genetic PCA analysis, incorporating
(Bonferroni post hoc tests, all P < 0.05, Figure 3). However, for allelic frequencies, revealed two distinct clusters along the
PCLINEAR 1−2 body depth differed between the age categories first axis (PC1 = 13.6%); the first cluster encompassing all
and a statistically significant interaction effect (Supplementary specimens collected in the Ratel River tributary (locality J) and
Table 1) was present between locality and age, indicating that the a small proportion of outlier individuals from locality C, H,
size-age relationship was locality specific. and I, with the second cluster representing all other sampled

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Diedericks et al. Directed Dispersal in Smallmouth Bass

FIGURE 3 | Graphs illustrating the mean and standard deviation for each locality with regards to (A) PCSHAPE1 (dorsal-ventral redistribution), (B) PCSHAPE2 (rounded
bodies, shortened caudal peduncle), (C) PCLINEAR1 (body depth), and (D) PCLINEAR2 (gape size). Different alphabetical letters above the bars indicate values with
statistically significant differences (Bonferroni post hoc test; P < 0.05), while identical letters indicate no significant differences among means. The fish outline
drawings on the left of graph (A,B) depict the variation in fish body shape for PCSHAPE1 and PCSHAPE2 , respectively. The light blue line representing the average
shape for all fish, while the dark blue line represents the upper and lower body shape extremity (scale factor set to 0.08 and – 0.08, respectively).

FIGURE 4 | Graphs illustrating the relationship between (A) body depth (PCLINEAR1 ) and (B) gape size (PCLINEAR2 ) and the environmental variables (PCENVIRONMENT1 )
for each sampled locality (A – J).

localities (Supplementary Figure 4). Less variation was observed greater than 60 km (all P < 0.197; Figure 6). These results
for the second axis (PC2 = 6.6%; Supplementary Figure 4). remained the same when removing locality J from the analyses
The Bayesian clustering method implemented in STRUCTURE (results not shown).
identified two genetic clusters [K = 2, LnP(D) = −2461.26;
Figure 5 and Supplementary Figure 5], one encompassing
nearly all of the Ratel tributary specimens, and the other Connectivity and Dispersal Among
cluster representing all other localities, corroborating the genetic Populations
PCA results. Both spatial autocorrelation analyses revealed that A significant association (rxy = 0.462, P = 0.001, R2 = 0.214)
M. dolomieu specimens displayed significantly more genetic between geographical distance and genetic divergence was
structuring in the shortest distance classes (up to ∼18 km) observed across all sampled localities (Supplementary Figure 6).
than what is to be expected under the null model (Figure 6; Nine first generation migrants were detected with GENECLASS
all P < 0.007). In contrast, pairwise multilocus genotypes 2.0; two each for localities A (A3, A9), I (I4, I5) and J
were significantly less genetically similar for all distance classes (J9, J18) and one each for localities C (C14), D (D19) and

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Diedericks et al. Directed Dispersal in Smallmouth Bass

TABLE 2 | Genetic diversity measures (n = number of genotyped individuals; Na = number of alleles; AR = allelic richness for a minimum of 15 individuals;
HE = expected heterozygosity, HO = observed heterozygosity; FIS = inbreeding coefficient) for nine microsatellite loci amplified for each of the seven localities.

Locality

A B C D H I J

Mdo3 n 19 20 20 20 20 22 18
Na 4 2 3 3 3 3 2
AR 3.659 2.000 2.978 2.700 2.700 2.999 2.000
HE 0.289 0.508 0.581 0.422 0.396 0.537 0.413
HO 0.21 0.50 0.35 0.45 0.50 0.36 0.22
FIS 0.276 0.016 0.404 −0.069 −0.271 0.328 0.469

Mdo4 n 15 20 19 17 18 21 14
Na 3 2 3 4 2 3 4
AR 2.998 2.000 2.997 3.620 2.000 2.999 4.000
HE 0.301 0.467 0.553 0.223 0.5 0.598 0.468
HO 0.20 0.60 0.58 0.24 0.61 0.43 0.36
FIS 0.344 −0.295 −0.048 −0.058 −0.23 0.289 0.244

Mdo5 n 18 19 20 20 20 21 17
Na 3 2 3 3 3 5 4
AR 2.733 2.000 2.995 3.000 3.000 4.561 3.824
HE 0.160 0.478 0.496 0.619 0.673 0.713 0.570
HO 0.056 0.421 0.350 0.600 0.700 0.571 0.588
FIS 0.660 0.122 0.300 0.032 −0.041 0.203 −0.032

Mdo7 n 19 20 20 20 20 21 18
Na 5 3 4 4 4 4 4
AR 4.673 2.999 3.978 4.000 3.978 3.991 3.778
HE 0.723 0.614 0.671 0.756 0.695 0.731 0.621
HO 0.632 0.550 0.750 0.750 0.800 0.667 0.389
FIS 0.134 0.107 −0.122 0.009 −0.156 0.089 0.380

Mdo8 n 19 20 20 20 20 22 18
Na 2 3 4 4 5 6 3
AR 2.000 2.700 3.400 3.694 4.377 5.729 2.954
HE 0.512 0.483 0.458 0.453 0.456 0.722 0.298
HO 0.53 0.40 0.50 0.40 0.45 0.64 0.22
FIS −0.029 0.176 −0.095 0.119 0.014 0.121 0.261

Mdo9 n 19 20 20 20 20 22 18
Na 2 4 5 4 4 7 13
AR 2.000 3.700 4.655 3.100 3.915 6.018 11.789
HE 0.273 0.676 0.592 0.146 0.686 0.677 0.917
HO 0.211 0.800 0.600 0.150 0.550 0.772 0.944
FIS 0.234 −0.190 −0.013 −0.027 0.202 −0.146 −0.030

Mdo10 n 19 20 20 20 20 22 18
Na 3.000 2.000 2.000 3.000 2.000 2.000 4.000
AR 2.673 2.000 2.000 2.700 1.999 2.000 3.725
HE 0.152 0.385 0.328 0.535 0.224 0.474 0.303
HO 0.105 0.400 0.300 0.650 0.150 0.545 0.333
FIS 0.314 −0.041 0.088 −0.223 0.337 −0.156 −0.103

Mdo11 n 18 20 20 20 19 22 18
Na 5 2 3 5 3 3 6
AR 4.55 2.00 3.00 4.10 3.00 3.00 5.47
HE 0.463 0.358 0.545 0.469 0.514 0.677 0.606

(Continued)

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Diedericks et al. Directed Dispersal in Smallmouth Bass

TABLE 2 | (Continued)

Locality

A B C D H I J

HO 0.50 0.45 0.65 0.55 0.63 0.55 0.61

FIS −0.081 −0.267 −0.199 −0.177 −0.238 0.197 −0.008

Lma21 n 18 19 20 20 20 21 17
Na 4 4 3 4 7 6 5
AR 4.00 3.72 3.00 3.70 6.23 5.30 4.64
HE 0.705 0.603 0.504 0.483 0.7 0.612 0.41
HO 0.833 0.579 0.450 0.550 0.950 0.476 0.294
FIS −0.189 0.041 0.109 −0.142 −0.370 0.226 0.289

Significant values, after 1,000 permutations, are represented in bold (P < 0.05).

H (H2). No migrant individuals were detected in locality B. concerning invasive species, have attempted to unravel the effect
The majority of these first-generation migrants were males directed dispersal may have on fine scale genetic- and phenotypic
(6/9), with 8/9 migrants belonging to the 2–3-year age class variation among populations. In the present study, we used
(Supplementary Data Sheet 1). All migrants originated from the invasive smallmouth bass, M. dolomieu, as study organism
either locality H, I or J. The assignment test revealed that to investigate the influence of individual dispersal on the fine
54% of all individuals were correctly assigned when considering scale genetic- and phenotypic variation along a river course.
the locality of highest probability (Figure 5). The majority of Our results revealed a strong correlation between phenotype
misassigned individuals were collected from localities B, C, D, and environment, independent of genetic variation. Although
and H (Figure 5). All nine first generation migrants formed part significant genetic population differentiation was detected among
of the misassigned individuals. populations, limited dispersal (as inferred from microsatellite
The first CCA revealed that the overall morphology data) suggests that matching habitat choice is unlikely to have
corresponded significantly to environmental variation (F = 3.47, contributed to the successfully establish of the smallmouth bass
P = 0.001; Figure 7). River slope (RS: F = 10.39, P = 0.001), and in the Olifants River.
to a lesser extent flow accumulation (FA: F = 2.45, P = 0.02)
and annual mean temperature (BIO1: F = 2.50, P = 0.02) were Correlates in Morphological and
statistically significant correlates of variation in morphology. The Environmental Variation
partial CCA, accounting for the additional effects of genetic
Combining morphometric measures with environmental
variation, was once again statistically significant (F = 2.51,
variables obtained from a near-global database, our results
P = 0.001), but revealed less influence of climatic variation
support the prediction that comparable environments will have
on morphology (RS: F = 6.67, P = 0.001; FA: F = 2.31,
similar phenotypes, particularly with reference to the linear
P = 0.03; BIO1: F = 1.95, P = 0.06; Figure 7), confirming
morphometric measures, with both body depth (PCLINEAR 1 )
the lack of genetic influence on the morphology. When
and gape size (PCLINEAR 2 ) being correlated to environmental
accounting for the effect of dispersal and genetics∗ dispersal,
variables (PCENVIRONMENT 1 ; Figure 4). Despite the significant
however, the morphology-environment correspondence was no
interaction effect between locality and age, examination of
longer statistically significant (dispersal: F = 1.08, P = 0.30;
the within population variation revealed that all individuals
genetics∗ dispersal: F = 0.93, P = 0.53; Figure 7). In these two
belonging to locality A had high scores for PCLINEAR1 regardless
partial CCAs the morphology-environmental correspondence
of age (Supplementary Figure 2). No significant correlation
became weak (dispersal – RS: F = 2.38, P = 0.02; FA: F = 0.82,
was, however, detected between any of the environmental
P = 0.05; BIO1: F = 0.99, P = 0.35; genetics∗ dispersal – RS:
variables and body shape (PCSHAPE 1−4 ), likely due to the large
F = 1.98, P = 0.04; FA: F = 0.81, P = 0.57; BIO1: F = 0.70, P = 0.68).
amount of within-locality variation. The arching of the body, as
described by PCSHAPE 1 , may have been due to slight differences
in specimen posture during landmark capture, as shown by
DISCUSSION Valentin et al. (2008).
The Jan Dissels tributary (localities A – C) is characterized
Lotic systems in hydrologically diverse environments, such as by high-flow environments, evident from the steeper slope and
in Mediterranean climate regions, are known to be spatially the higher percentage of pebbles and rocks (CFRVOL; Johnson,
and temporally variable (Winemiller et al., 2010; Cooper et al., 2004). It is thus not surprising that M. dolomieu from locality
2013). Thus, in order to persist in such changing environments, A (and subsequently localities B and C) were significantly more
species either need to adapt or move to more suitable habitats streamlined when compared to the other populations (Figure 3),
when changes occur. However, despite directed dispersal gaining supporting the hypothesis of Langerhans (2008) stating that
attention in the literature, few studies to date, particularly those streamlined fish will be present in high-flow environments, as this

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Diedericks et al. Directed Dispersal in Smallmouth Bass

FIGURE 5 | A graphical representation of the seven sampled localities used in the genetic analyses (A – D, H – J). The percentage correctly assigned individuals,
obtained from GENECLASS 2.0, for each sampled locality is depicted with a pie chart, with colors corresponding to those in the legend on the right. The
STRUCTURE plot represents all seven sampled localities, with each line in the plot corresponding to an individual within that sampled locality. Colors represent the
proportion of an individual’s genotype assigned to a given genetic cluster (K = 2).

body shape promotes steady swimming in fast flowing waters. together. Relative gape size was found to decrease with a decrease
Despite the distinct morphology of the fish collected in the in clay content mass (CLYPPT; Figure 4), and consequently an
Ratel tributary (locality J – PCSHAPE 2 , and to a lesser extent increase in coarse fragments. Invertebrates, especially crabs, are
PCLINEAR 1 ; Figure 3), no association could be made with habitat known to prefer coarse substrate habitats situated in pristine,
(Figure 4). This is likely because of the broad scale environmental high flow environments (Zimmerman and Covich, 2003; DWA,
variables (1 km2 grid) used in the present study and the close 2006), as present in the Jan Dissels tributary. A smaller gape and
proximity of locality J to the main stem. Similarly, substantial consequently stronger suction (Carroll et al., 2004; Wainwright
variation between localities, though not statistically significant, et al., 2007; Day et al., 2015), might be advantageous in this
was observed in gape size (PCLINEAR 2 ; Figure 3), with localities environment as a stronger suction is required to feed on benthic
A – C, characterized by a relatively smaller gape size, clustering prey items, such as crabs (Day et al., 2015). In contrast, a relatively

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Diedericks et al. Directed Dispersal in Smallmouth Bass

FIGURE 6 | Multiallelic correlograms (blue line) showing the spatial genetic structure of M. dolomieu across two distance classes (10 and 20 km). The 95% null
hypothesis confidence intervals are indicated by the red dotted lines. Positive values represent individuals more genetically similar than expected in a given distance
class, while negative values imply that individuals in that distance class are less genetically similar than expected. The value in brackets denote the number of
pairwise comparisons. The asterisk denotes the statistically significant pairwise relatedness in a specific distance class.

large gape is better suited for ram feeding and predating on fish These findings are in line with previous work, describing
in the water column (Carroll et al., 2004; Wainwright et al., 2007; riverine M. dolomieu inhabitants as sedentary, establishing and
Day et al., 2015). This may well be the case in the mainstem of guarding home ranges and displaying nest site fidelity (Todd
the Olifants River system, as numerous co-occurring fish species and Rabeni, 1989; Ridgway and Shuter, 1996). In contrast to
are present (Van der Walt et al., 2016). Moreover, the fact that our prediction, high levels of within locality variation were
M. dolomieu from the Jan Dissels tributary have more fusiform observed. This can potentially be explained by two alternative
bodies compared to the other localities further supports this hypotheses, as suggested by Barluenga and Meyer (2005).
notion, as steady swimming is needed to get close enough to Firstly, a large heterogenous lineage of smallmouth bass could
benthic prey (Sass and Motta, 2002; Higham, 2011). In contrast, have colonized the Olifants River, differentiating into several
thrust and maneuverability, associated with relatively deep bodies groups along the diverse river course. Secondly, multiple
(as seen within localities D – J; Figure 4), provides M. dolomieu genetically diverse lineages of smallmouth bass colonized the
with a fast approach and attack, essential to capture prey in the Olifants River, homogenizing the gene pool post introduction.
water column (Sass and Motta, 2002; Tran et al., 2010). Considering M. dolomieu’s invasion history and the supposedly
multiple introductions of smallmouth bass into South Africa,
and likely the Olifants River system (Diedericks et al., 2018a),
Population Structuring and Connectivity the latter hypothesis seems most probable. Moreover, the
Among Micropterus dolomieu existence of a Wahlund effect (Wahlund, 1928), i.e., the
Populations presence of (cryptic) cohorts in what is believed to be one
In the present study, we predicted that, following directed genetically homogeneous sample, further supports the hypothesis
dispersal, one would observe marked population structuring of multiple introductions. The underlying causes for a Wahlund
and little within population variance. Our results corroborate effect are thought to be geographic barriers and genetic drift,
this to some extent, as significant population differentiation although relatedness and inbreeding could also contribute
was detected. However, this was most likely a result of IBD (Castric et al., 2002). Several aspects of the current study system
(Supplementary Figure 6), with more genetic structuring than are in line with the characteristics of a Wahlund effect. Firstly,
expected over short distances, and less genetic structuring the presence of a dispersal barrier, the Clanwilliam Dam sluice
than expected over large distances, as revealed by the spatial gates, prohibits movement for fish from localities A – C to the
autocorrelation (Figure 6). Furthermore, the low number of main stem. Secondly, genetic drift could have been promoted
first-generation migrants detected further support this notion. through sudden immigration, as would be expected during an

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Diedericks et al. Directed Dispersal in Smallmouth Bass

FIGURE 7 | The canonical correspondence analysis biplots showing the relationship between morphological traits and environmental variables (A) without
considering genetics, (B) taking genetic variation into account, (C) taking dispersal (via gene flow) into account, (D) considering both genetic variation and dispersal.
Five environmental variables representing river topology, soil classification and hydroclimate were used, namely: annual mean temperature – BIO1, annual
precipitation – BIO12, average river slope – RS, flow accumulation – FA, and coarse fragments volumetric across sub-catchment – CFRVOL. Morphological trait
abbreviations correspond to those used in Table 1.

introduction event (Lee, 2002). Thirdly, as fish are known to the assignment test showed limited dispersal from the Ratel to
shoal with kin (Brown and Brown, 1996; Gerlach et al., 2001; downstream populations despite the absence of any geographical
Castric et al., 2002; Dehais et al., 2010) it is highly probable barriers. Numerous studies have revealed similar patterns. For
that genetically related individuals were sampled in the present example, higher genetic differentiation was found in introduced
study, as suggested by the similarity in age classes within each smallmouth bass inhabiting the tributaries of the Susquehanna
locality (Supplementary Data Sheet 1). Lastly, the high levels River basin compared to the main stem (Schall et al., 2017). In
of inbreeding detected could be ascribed to non-random mating, addition, Hendry et al. (2002) found high genetic divergence
driven by nest site fidelity (Dehais et al., 2010), a trait displayed by and little gene flow among stickleback populations inhabiting
smallmouth bass (Todd and Rabeni, 1989; Ridgway and Shuter, an inlet stream and a lake. Likewise, Carlsson et al. (1999)
1996). Despite the aforementioned, the Ratel tributary (locality J) demonstrate fewer brown trout exchanges between a tributary
was shown to be genetically distinct when compared to the rest and main stem than within the main stem itself. Tributaries
of the individuals, as suggested by the STRUCTURE and genetic are often ecologically differentiated thereby supporting locally
PCA results (Figure 5 and Supplementary Figure 4). Moreover, adapted populations that rarely disperse into the main stream

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Diedericks et al. Directed Dispersal in Smallmouth Bass

(Dehais et al., 2010). In contrast to the Ratel and Jan Dissels DATA AVAILABILITY STATEMENT
tributaries which sustain permanent water flow, individuals
inhabiting the mainstem of the Olifants River face the The datasets presented in this study can be found in the
risk of becoming trapped as sections of the river become Supplementary Material.
disconnected and dry up during summer. This may force
M. dolomieu to disperse either up- (locality J) or downstream
(locality D and subsequently A-C if the sluice gates are
ETHICS STATEMENT
opened) to other freshwater habitats with better environmental
conditions (Whitledge et al., 2002; Westhoff et al., 2016), and The animal study was reviewed and approved by the Research
could ultimately result in the limited population structuring Ethics Committee: Animal Care and Use (REC: ACU),
within the main stem. Stellenbosch University.

CONCLUSION
AUTHOR CONTRIBUTIONS
The results of our study reveal distinct genetic and morphological
differences between populations of M. dolomieu. On the one GD, SH, OW, and CH contributed to conception and design
hand, a strong correlation was found between morphological of the study. GD and CB conducted the sampling and took all
traits and environmental conditions, irrespective of the observed the linear measurements. GD conducted all the genetic lab work
genetic variation among the populations. On the other hand, and analyses, landmarked all specimens, and wrote the first draft
the populations were genetically differentiated due to isolation- of the manuscript. GD and OW aged the fish. CB performed
by-distance (IBD). This IBD pattern suggests that gene flow, all the statistical analysis. All authors contributed to manuscript
and thus dispersal, is more likely to occur between closely revision, read, and approved the submitted version.
situated populations than those at greater spatial distances.
Limited dispersal between habitats could result from matching
habitat choice (Edelaar et al., 2008), provided individuals have
the opportunity to select between different habitat types. In
FUNDING
our study system, such instances appeared to be rare as
This work was supported by the Department of Science
habitats of neighboring localities were often very similar, or
and Technology (DST) and National Research Foundation
separated by a barrier (e.g., Jan Dissels). A notable exception
(NRF) of South Africa (CH: 89967 and 109244; OW: 110507
is the Ratel tributary, which represents a morphological and
and 109015) and the DST-NRF Centre of Excellence for
genetically distinct population within the Olifants River. The
Invasion Biology (GD).
strong genetic structuring observed within the tributary appears
to be non-random (i.e., directed gene flow from the neighboring
populations toward the tributary as revealed by the migrant
analysis; Figure 5), reflecting the proposed genetic pattern ACKNOWLEDGMENTS
suggested by the matching habitat choice hypothesis (Edelaar
et al., 2008; Nicolaus and Edelaar, 2018). In loving memory of OW who passed away on 14 November 2020
In conclusion, our study highlights the importance of gene while chasing fish in mountain streams. We thank Liz Alter and
flow and dispersal in shaping the fine scale population genetic Erika Rubenson for their useful comments and suggestions.
variation, particularly with reference to invasive species. The
use of whole genome markers such as SNPs (Tiffin and Ross-
Ibarra, 2014), coupled with more comprehensive spatial sampling SUPPLEMENTARY MATERIAL
schemes and detailed spatio-temporal environmental data, will
be pivotal to understand the relative importance of directed The Supplementary Material for this article can be found
dispersal, local adaptation, phenotypic plasticity and random online at: https://www.frontiersin.org/articles/10.3389/fevo.2021.
genetic differentiation for trait variation. 790829/full#supplementary-material

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Behavioural thermoregulation and bioenergetics of riverine smallmouth bass Copyright © 2022 Diedericks, Broeckhoven, von der Heyden, Weyl and Hui. This
associated with ambient cold-period thermal refuge. Ecol. Freshw. Fish 25, is an open-access article distributed under the terms of the Creative Commons
72–85. doi: 10.1111/eff.12192 Attribution License (CC BY). The use, distribution or reproduction in other forums
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on specific daily metabolic demand and growth scope of sub-adult and adult and that the original publication in this journal is cited, in accordance with accepted
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