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The invasion of Patagonia by Chinook salmon (Oncorhynchus tshawytscha): Inferences from mitochondrial DNA patterns

  • Instituto Patagónico para el Estudio de los Ecosistemas Continentales (IPEEC-CONICET)

The invasion of Patagonia by Chinook salmon (Oncorhynchus tshawytscha): Inferences from mitochondrial DNA patterns

Abstract and Figures

The Chinook salmon Oncorhynchus tshawytscha, which was introduced deliberately in Chile four decades ago for sport fishing and aquaculture, represents a rare example of a successful translocation of an anadromous Pacific salmon into the southern Hemisphere, offering a unique opportunity to examine the role of introduction history and genetic variability in invasion success. We used historical information and mitochondrial displacement loop sequences (D-loop) from seven colonized sites in Chile and Argentina and from native and naturalized Chinook salmon populations to determine population sources and to examine levels of genetic diversity associated with the invasion. The analysis revealed that the Chinook salmon invasion in Patagonia originated from multiple population sources from northwestern North America and New Zealand, and admixed in the invaded range generating genetically diverse populations. Genetic analyses further indicated that the colonization of new populations ahead of the invasion front appear to have occurred by noncontiguous dispersal. Dispersal patterns coincided with ocean circulation patterns dominated by the West Wind Drift and the Cape Horn Currents. We conclude that admixture following multiple introductions, as well as long-distance dispersal events may have facilitated the successful invasion and rapid dispersal of Chinook salmon into Patagonia.
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The invasion of Patagonia by Chinook salmon (Oncorhynchus
tshawytscha): inferences from mitochondrial DNA patterns
C. M. Riva Rossi M. A. Pascual E. Aedo Marchant
N. Basso J. E. Ciancio B. Mezga
D. A. Ferna
´ndez B. Ernst-Elizalde
Received: 11 May 2012 / Accepted: 21 November 2012 / Published online: 28 November 2012
ÓSpringer Science+Business Media Dordrecht 2012
Abstract The Chinook salmon Oncorhynchus tshawyts-
cha, which was introduced deliberately in Chile four dec-
ades ago for sport fishing and aquaculture, represents a rare
example of a successful translocation of an anadromous
Pacific salmon into the southern Hemisphere, offering a
unique opportunity to examine the role of introduction
history and genetic variability in invasion success. We used
historical information and mitochondrial displacement loop
sequences (D-loop) from seven colonized sites in Chile and
Argentina and from native and naturalized Chinook salmon
populations to determine population sources and to exam-
ine levels of genetic diversity associated with the invasion.
The analysis revealed that the Chinook salmon invasion in
Patagonia originated from multiple population sources
from northwestern North America and New Zealand, and
admixed in the invaded range generating genetically
diverse populations. Genetic analyses further indicated that
the colonization of new populations ahead of the invasion
front appear to have occurred by noncontiguous dispersal.
Dispersal patterns coincided with ocean circulation pat-
terns dominated by the West Wind Drift and the Cape Horn
Currents. We conclude that admixture following multiple
introductions, as well as long-distance dispersal events may
have facilitated the successful invasion and rapid dispersal
of Chinook salmon into Patagonia.
Keywords Human-mediated invasions
Exotic salmonids Multiple introductions
Admixture Long-distance dispersal
Patagonia, at the southern end of South America
(39°–56°S), is a vast territory surrounded by the Pacific (to
the west) and Atlantic (to the east) Oceans, which supports
some of the last unpolluted freshwater ecosystems on
Earth. Patagonia exhibits relatively low species richness
and high levels of endemism (Dyer 2000; Pascual et al.
2002; Cussac et al. 2009; Habit et al. 2012), which provide
ideal conditions for the introduction of semiaquatic (e.g.,
mink and beaver) and aquatic exotic species, including
trout and salmon. Salmonids were widely translocated into
Patagonian basins from their native ranges in the Northern
Hemisphere for both recreational and aquaculture pur-
poses. Most attempts to transplant anadromous species,
which breed in fresh water and migrate to the ocean to
C. M. Riva Rossi (&)M. A. Pascual J. E. Ciancio
Grupo de Estudios de Salmo
´nidos Ana
´dromos (GESA), Centro
Nacional Patago
´nico (CENPAT-CONICET), Blvd. Brown 2915,
9120 Puerto Madryn, Chubut, Argentina
E. Aedo Marchant
Centro Trapananda, Universidad Austral de Chile, Coyhaique,
XI Regio
´n de Ayse
´n, Chile
N. Basso
Laboratorio de Biologı
´a Molecular, Centro Nacional Patago
(CENPATCONICET), Blvd. Brown 2915, 9120 Puerto Madryn,
Chubut, Argentina
B. Mezga
Facultad de Ciencias Naturales, Universidad Nacional de la
Patagonia, 9120 Puerto Madryn, Chubut, Argentina
D. A. Ferna
Centro Austral de Investigaciones Cientı
´ficas (CADIC-
CONICET), 9410 Ushuaia, Tierra del Fuego, Argentina
B. Ernst-Elizalde
Departamento de Oceanografı
´a, Universidad de Concepcio
´n, VIII Regio
´n del Biobı
´o, Chile
Genetica (2012) 140:439–453
DOI 10.1007/s10709-012-9692-3
feed, to locations around the world have failed. However,
several anadromous salmonids have been particularly
successful in Patagonia (Pascual and Ciancio 2007).
Established populations of anadromous rainbow On-
corhynchus mykiss and brown trout Salmo trutta were
reported in Atlantic rivers of Southern Patagonia at the
beginning of the twentieth century, and Chinook salmon
Oncorhynchus tshawytscha, which was more recently
introduced, is actively colonizing both Atlantic and Pacific
river basins throughout the region (Ciancio et al. 2005;
Correa and Gross 2008; Ferna
´ndez et al. 2010).
The successful establishment of Chinook salmon in
Patagonian rivers began in the late 1970s as a consequence of
escapees from fish farms in Chile. Most aquaculture efforts
were directed at breeding Atlantic Salmo salar and Coho
salmon Oncorhynchus kisutch. However, Chinook salmon,
the species with the least introduction effort in Patagonia was
shown to be the most successful at colonizing glacial-fed,
cold water Pacific and Atlantic river basins (Soto et al. 2007;
Pascual et al. 2009). This is the second example of successful
introduction and spread of Chinook salmon in the Southern
Hemisphere, following colonization of New Zealand
streams from plantings performed during the late 1800s
(Quinn et al. 2001), and underlies the remarkable evolu-
tionary potential of this species for colonization, establish-
ment, and subsequent range expansion into new habitats
(Ciancio et al. 2005; Correa and Gross 2008).
Chinook salmon exhibit wide variability in life history
traits, a characteristic influenced by genetic and environ-
mental factors (Healey 1991; Quinn et al. 2001) that may
result in increased invasive potential. Debate is ongoing to
establish if this variation provided Chinook salmon with
the ancestral capacity to invade novel habitats (i.e., pre-
adaptation), and/or if the variation resulted from rapid
selective responses to local conditions (i.e., local adapta-
tion) (Ciancio et al. 2005; Correa and Gross 2008). Reci-
pient community attributes, such as suitable environmental
conditions and low species diversity (e.g., few predators
and competitors), and the unique characteristics of Pata-
gonian aquatic ecosystems have also been suggested as
responsible for invasive success (Pascual et al. 2002;
Correa and Gross 2008; Schro
¨der and Garcia de Leaniz
2011; Habit et al. 2012).
As with many other organisms, the role of genetic vari-
ation in the successful colonization, dispersal, and adapta-
tion of Chinook to novel habitats has received far less
attention than other factors. The capacity of a population to
respond to selection is proportional to the level of genetic
variation, which in turn is affected by the number of
founders, or the number of introduction events. This led to a
hypothesis that any loss in genetic variability associated
with bottlenecks or founder effects during the natural col-
onization of a new habitat may compromise the adaptive
potential of a population to new environments (Sakai et al.
2001). However, studies of human-mediated introductions
usually report successful invasions exhibiting similar or
augmented levels of genetic variation compared with native
populations which are attributed to the introduction of large
numbers of individuals, multiple founding population of
diverse origins, or admixture (e.g., Astorga et al. 2008;
Consuegra et al. 2011). Through admixture, large levels of
variation can result in new genetic combinations associated
to novel physiological characteristics, which may facilitate
rapid adaptation to novel environments (Kolbe et al. 2004,
2008; Dlugosch and Parker 2008;Ha
¨nfling 2007).
Determining the attributes responsible for species’ inva-
sion success is challenging. Chinook salmon clearly dem-
onstrate increased success at colonizing and dispersing in
new environments relative to other anadromous salmonids.
One means to investigate the influence of different processes
that affect invasion success is to study the invasive species’
introduction history and the level of genetic variation of
invasive versus native populations (e.g., Le-Roux et al.
2011). Consequently, it may be possible to determine the
likely origins, the number of introduction events, and the
structure and connectivity of the invasive populations.
Introduction history and the invaders’ genetic composition
can subsequently be bridged with invasion success, aiding in
understanding the mechanisms that facilitate the establish-
ment and dispersal of non-native species in newly colonized
areas (Wares et al. 2005). In the present study, patterns of
genetic diversity among native and introduced Chinook
salmon populations were compared using the mitochondrial
control region (D-loop) to reconstruct the invasion origins
and dispersal patterns of this species.
Materials and methods
Introduction history
Review works of Basulto (2003) and Correa and Gross
(2008) were used to obtain Chinook salmon introduction
data into Chile and Argentina. We also reviewed unpub-
lished base-line data collected from two National Fisheries
Administration Offices from Chile: Subpesca (Subsec-
´a de Pesca,, and Sernapesca
(Servicio Nacional de Pesca,
These records indicated the earliest attempts to introduce
Chinook salmon in Chile dated back to 1886 from Paris,
France (from individuals native to California), and 1924
and 1930, from California, but the efforts were unsuccess-
ful. Additional imports were not reported for at least half a
century. However, with the onset of the commercial salmon
industry during the 1980s, salmon imports increased con-
siderably. Chinook salmon from the Cowlitz River, a
440 Genetica (2012) 140:439–453
tributary of the lower Columbia River basin in Washington
State, USA, and one stock derived from the Kalama River,
also a tributary of the lower Columbia River basin from the
University of Washington Hatchery, were introduced on
several occasions for ocean ranching in the Chiloe
´area near
Puerto Montt, Chile (Fig. 1a). From 1982 to 1988, male and
female gametes from these returns along with Chinook eggs
from the University of Washington were used to run a
ranching program in the southern channels of Chile’s XII
Region (49°–56°S), first based at the Santa Marı
´a (54°S),
and later at the Prat (51°S) River (Fig. 1a). Following 1987,
additional Chinook salmon from the Oregon coast, Puget
Sound in Washington State, and the Vancouver area in
British Columbia (Canada) were imported to the X Region
(39°–44°S) for experimental net pen rearing. By 1991,
Chilean aquaculture converted entirely to ocean net pens
and was performed almost exclusively in northern localities
along the X and XI Regions (44°–49°S), which imported
and reared stocks derived from the Vancouver and Puget
Sound areas. Additional strains from commercial stocks
were introduced and from New Zealand (of California ori-
gins) (Fig. 1b). Chinook salmon imports into Chile ceased
during the 2000s.
Beginning in the early 1980s, free-ranging Chinook sal-
mon were recorded in several Pacific basins in proximity to
the X and XII Regions, the primary introduction sites (Correa
and Gross 2008). The species was also reported in the
headwaters of two Pacific basins in Argentina: the Corco-
vado and Futaleufu
´Rivers (Grosman 1992) (Fig. 1a). Con-
currently, stray fish returns were recorded in the Caterina
River (50°S), a small river at the Santa Cruz River head-
waters, which drains into the Atlantic Ocean (Ciancio et al.
2005; Becker et al. 2007). During the 1990s, salmon pro-
duction increased as a result of net pen farming. Reports of
Chinook salmon originating from aquaculture facilities
continued, with strays occurring into several Pacific outlet
rivers in Chile and Argentina from 40°Sto45°S (Basulto
2003; Soto et al. 2007; Correa and Gross 2008; Di Prinzio
and Pascual 2008) (Fig. 1b). Documentation of Chinook
salmon strays rapidly intensified through the end of the 20th
into the beginning of the 21st centuries, including Chilean
Tolten (39°S) and Valdivia (40°S) Basin Rivers to the north,
the Baker (47°S), Pascua (48°S), and Serrano (51°S) Rivers
south of 45°S (Correa and Gross 2008), and the Beagle
Channel Rivers (54°S) in Tierra del Fuego (Ferna
´ndez et al.
2010). Most recently, local fishermen have reported Chinook
salmon in the Grande (53°S) and Gallegos Rivers (51°S), two
Atlantic basins famous for world-class sport fishery of sea-
run brown trout, and in the De las Vueltas River (49°S) in the
headwaters of the Santa Cruz River (Fig. 1).
Fig. 1 Introduction and colonization history of Chinook salmon in
Chile and Argentina (based on Correa and Gross 2008). The three
panels indicate different time periods since the first introduction to
Chile. Black symbol in panels a and b designate per site stockings
from a different geographic source: Vancouver area in British
Columbia (Va, square), Puget Sound area in Washington State (Pu,
up triangle), University of Washington (UW, down triangle), Cowlitz
River in Washington State (Co, diamond) Oregon Coast (Or, circle),
New Zealand (NZ, star), and Curaco de Ve
´lez (CdV, asterisk). The
shaded areas are basins, with rivers and lakes shown in a darker
shade, where free-ranging and spawning individuals have been
recorded (names of colonized basins only shown when first noted)
Genetica (2012) 140:439–453 441
Sampling and DNA techniques
Chinook salmon populations were sampled between Janu-
ary and March 2005 through 2009 from seven major
Chilean and Argentinean Patagonia basins, including two
original introduction sites: the Cobarde, a tributary of the
Simpson (44°S) and Prat (51°S) Rivers in Chile, and five
colonized rivers, including the Vargas, a tributary of the
Baker (47°S) and Serrano (51°S) Rivers in Chile, and
Corcovado (43°S), a tributary of the Palena River, which
flows into the Pacific Ocean, Caterina River (50°S) flowing
into the Atlantic Ocean, and the Ovando River (54°S)
emptying into the Beagle Channel in Argentina (Fig. 2c).
Gillnetting, carcass collection, and angling were used in
several stations along the watershed to obtain samples.
Tissue samples were also collected from 25 fish from a
small hatchery located at Pichicolo, near Puerto Mont in
the X Region (42°S), which maintains a local Chinook
salmon broodstock originally developed from Washington
State stocks.
Tissue samples were preserved in 95 % ethanol and
DNA was extracted following standard protocols (Sam-
brook and Russell 2001). PCR was performed to amplify a
highly variable segment of the mtDNA (D-loop) control
region using the following two primers: T07 (50-
CTTAACTCCCAAAGCTA-30) (designed by C. Riva
Rossi and E. Lessa, Universidad de la Repu
´blica, Monte-
video, Uruguay), and P2 (50-TGTTAAACCCCTAAAC-
CAG-30, Nielsen et al. 1994). PCR followed the protocol in
Nielsen et al. (1994). Amplification yielded 954 base pairs
(bp) of high quality sequences from 141 individuals.
Amplified DNA templates were purified with the GENE-
CLEAN Purification Kit (Q BIOgene, Carlsbad, CA), and
20 ng of purified PCR product was used in cycle
sequencing reactions following ABI PRISM BigDye Ter-
minator protocols (Applied Biosystems, Foster City, CA).
Forward and reverse sequences were visualized on an ABI
PRISM 3130 automated sequencer at the Centro Nacional
Patagonico DNA Sequencing Laboratory and aligned with
the MEGA v.5 software (Tamura et al. 2011). Sequences
were imported into DNASP version 5 (Librado and Rozas
2009) to identify unique haplotypes and subsequently
deposited in GenBank under the accession numbers shown
in Table 1. In this study, our 954-bp haplotypes were
designated on the basis of homology to published
sequences. The standardized nomenclature for short hap-
lotypes (170-bp) in Chinook salmon followed the TSAX
format (where X is any integer designating the specific
haplotype), and longer haplotypes (414-bp) included the
name of short haplotypes that comprised the long haplo-
type, plus a haplotype-specific suffix (e.g., TSA1A is a long
haplotype that includes the short TSA1 haplotype).
Reported sequences from our study included an additional
haplotype-specific suffix determined by observation order
(e.g., longer haplotypes TSA10.1 to TSA10.3 comprise the
published TSA10 haplotype, Table 1).
Genetic analysis
The origins of introduced populations were determined
using Chinook salmon published sequence data from across
the species native and naturalized ranges: California
(Nielsen et al. 1994,1998; Williamson and May 2007),
Alaska to California (Martin et al. 2010) and New Zealand
(Quinn et al. 1996). We also included short sequences
previously recovered by Becker et al. (2007) from the
University of Washington stock. These studies were con-
ducted using smaller D-loop fragments (170-bp: Nielsen
et al. 1994; Quinn et al. 1996; Becker et al. 2007; 414-bp:
Martin et al. 2010) which were nested within the 954-bp
segment of mtDNA we sequenced. Therefore, to compare
with the most currently published D-loop haplotypes our
sequences were trimmed to 414-bp. To infer whether our
sampling efforts were sufficient, we used haplotype esti-
mation curves to estimate haplotype diversity in each range
(native, New Zealand and Patagonia) and to quantify the
effects of sampling effort on haplotype diversity. Specifi-
cally, we used the program ESTIMATES 8.0 (Colwell
2005) in order to estimate how many more haplotypes we
would expect to find if the sampling effort were increased,
given the existing data and sampling information. Samples
were randomized 1,000 times without replacement. The
following estimators for the total number of haplotypes to
be expected, and their respective confidence intervals
(where applicable), were extracted: Chao 1 and Chao 2
(Chao 1987), Jackknife 2 (Smith and van Belle 1984) and
Michaelis–Menten (Colwell and Coddington 1994).
With the short 414 bp D-loop segment, we examined
patterns of genetic similarity in haplotype frequencies
among native and non-native populations using a Multi-
dimensional Scaling (MDS) analysis as implemented in the
software R version 2.15 (R Development Core Team,
2012). The non-native population sources were also infer-
red on the basis of the geographic distribution of haplo-
types in the native range and phylogeographic relationships
among haplotypes. We used the TCS 1.3 program (Clem-
ent et al. 2000) to build a haplotype network (95 % sta-
tistical parsimony network). Haplotype networks better
illustrate genetic divergence at the intra-specific level,
particularly in cases where multiple haplotypes derive from
a single ancestral sequence (Templeton et al. 1992).
Population genetic analyses were conducted using the
software package ARLEQUIN 3.11 (Excoffier et al. 2005),
except where noted. Analyses of introduced populations
were performed on data for the full 954-bp long
442 Genetica (2012) 140:439–453
haplotypes. We estimated haplotype number, gene diver-
sity (h), and nucleotide diversity (p) among locations
within the non-native range, which were compared with
genetic diversity values reported for native populations
using Welch’s two-sample ttest in the statistical program
R. We further examined the distribution of genetic varia-
tion among and within populations using Analyses of
Molecular Variance (AMOVA; Excoffier et al. 1992). We
conducted separate AMOVAS accounting for pairwise
mutational differences between haplotypes (U
) (Weir
and Cockerham 1984; Excoffier et al. 1992) on populations
in the native range and for the introduced Patagonia pop-
ulations and significance was determined with 10,000
permutations. Genetic differentiation between population
pairs across the introduced range, with the exception of
Corcovado River (where we had a sample size of N =4),
was also investigated using an exact test, where haplotype
frequencies were compared with a random distribution
(Raymond and Rousset 1995). Pvalue significance was
computed with 10,000 permutations. A modified False
Discovery Rate procedure (B-Y FDR, Benjamini and
Yekutieli 2001) was applied to correct for multiple pair-
wise comparisons by adjusting significance levels (Narum
2006). We subsequently tested for a relationship between
population differentiation ([U
/(1 -U
)]), and geo-
graphical distance (in km) using a Mantel test of isolation
by distance (IBD) based on Slatkin’s linearized U
(with 10,000 randomizations).
Fig. 2 Locations of Chinook salmon populations analyzed in this
study and geographic distribution of mtDNA control region haplo-
types from throughout the species’ native (a), naturalized (b), and
introduced ranges (c) in Patagonia. Gray-scale shading designate
unique haplotypes and their frequencies within each population.
Haplotypes not present in the introduced range were pooled. In athe
native Chinook salmon range was divided into three regions (north,
central, and south) depicted on the left side of the figure based on
Martin et al. (2010) (see Table 2for population names). In
bhaplotypes TSA1a and 10 were pooled. In clong haplotype
frequencies of TSA10.1 to TSA10.3 recovered in this study are
represented by a unique shade, but their relative contributions are
indicated by their haplotype-specific suffix designation
Genetica (2012) 140:439–453 443
Origins of introduced Chinook salmon
Five ‘‘short’’ haplotypes were identified when sequences
were trimmed down to the 414-bp segment, all of which
corresponded to the following published haplotypes:
TSA6, TSA10, TSA14, TSA15, and TSA17 (Tables 1,2;
Fig. 2). Haplotype TSA10 (Martin et al. 2010) was detec-
ted at all locations across the native range and included
shorter haplotype CH1 identified by Nielsen et al. (1994)
from California samples, which was recovered by Quinn
et al. (1996) in New Zealand samples. It also included
shorter haplotypes SC1 and WA1, identical to haplotype
CH4 (Nielsen et al. 1994), identified in the Caterina River,
the UW stock (Becker et al. 2007) and the Ovando River
´ndez et al. 2010). Haplotypes TSA14, described
from Willamette River samples (a major tributary of the
Columbia River in Oregon), and TSA15, detected in Cal-
ifornia samples (Martin et al. 2010), included shorter
haplotype TSA3 found in California and New Zealand
Chinook samples (Nielsen et al. 1994; Quinn et al. 1996;
Nielsen et al. 1998) and in the Ovando River in Argentina
´ndez et al. 2010). Haplotype TSA17 was recovered
in populations from Russia to Washington (Martin et al.
2010), and haplotype TSA6 (Nielsen et al. 1998) from
California Chinook samples was identical to haplotype
WA2 in the UW stock (Becker et al. 2007). This haplotype
was also recovered in the Pichicolo sample, a Chilean
hatchery founded by Washington State stocks. In aligning
the native and non-native mtDNA sequences, a discrepancy
was found at position 1,032 (Table 1, based on the base
pair positions given by Digby et al. (1992) for Oncorhyn-
chus mykiss). In evaluating Nielsen et al. (1994), Becker
et al. (2007) assigned an A to the haplotypes at this position
for all but the Caterina River and UW samples, where a G
was assigned at position 1,032. However, Nielsen et al.
(1998) indicated a G at position 1,032, consistent with all
other available published sequences for Chinook salmon.
All the sequences generated in this study have a G at that
position giving not support for a polymorphism.
Haplotype richness (estimated via rarefaction curves of
number of haplotypes per number of locations sampled) for
each region indicate that both New Zealand and Patagonia
introduced ranges have been well-sampled and the detected
number of haplotypes is near the asymptote of the predicted
total number of haplotype in the system (Fig. 3). In contrast,
sampling throughout the native range has not yet reached this
asymptote and additional diversity may be discovered with
additional sampling (Fig. 3). Extrapolation from the data,
with re-sampling, provided estimates of the total number of
native range haplotypes between 18 (Chao 1) and 25 (Chao 2)
(Table 2), compared to the 17 detected by Martin et al. (2010).
The MDS analysis based on haplotype frequencies
indicated the presence of three main distinct clusters
(Fig. 4). Among native range populations, Chinook salmon
from Russia and Alaska were placed close to Washington
populations. The populations from California formed a
fairly compact cluster together with naturalized popula-
tions from New Zealand and were well separated from the
remaining native populations. The non-native populations
fell into a third cluster along with the University of
Washington stock and the populations from British
Columbia and Oregon. Within this cluster, those popula-
tions with high frequency of haplotype TSA10 (Cobarde,
Prat, Caterina and Serrano Rivers) were closest to the
University of Washington stock and British Columbia
whereas those with higher frequency of haplotype TSA14
(Vargas, Corcovado and Ovando) were closest to the
Willamette River population in Oregon. The 95 % parsi-
mony TCS haplotype network revealed limited phylogeo-
graphic structure based on the mtDNA D-loop across the
native Chinook salmon range (Fig. 5). Native species
populations consisted of a relatively large number of clo-
sely related haplotypes. The four most common (TSA 17,
TSA 1B, TSA 1A, and TSA10) were detected in the central
geographic region of the native range. Two of these hap-
lotypes (TSA 1A and TSA 10) were not identified in the
northern region of the range, and the other two haplotypes
(TSA 17 and TSA 1B) were not detected from the southern
geographic area. Additional haplotypes were found exclu-
sively in the northern (TSA 20 and TSA 21), central
(TSA11, 12, 13, 16), or southern regions (TSA 2A and
TSA 15) (Martin et al. 2010). Introduced populations
exhibited fewer haplotypes than native populations (five vs.
12 for the shorter fragment, respectively) and were dis-
tributed in different sectors of the network, with haplotypes
identified in different geographic regions within the native
Genetic variation and structure within the introduced
The longer 954-bp fragment resulted in seven distinct hap-
lotypes: TSA10.1 to TSA10.3, TSA6.1, TSA14.1, TSA15.1,
and TSA17.1 (see Table 1, Sampled Populations). Haplo-
type TSA10.1 was the most common (detected at all non-
native locations) and represented 54.2 % of the individuals.
High TSA10.1 frequency in the introduced area was con-
gruent with the predominance of the haplotype in various
locations across the native species range. The second most
frequent haplotype was TSA14.1, represented in 13.7 % of
the individuals recorded at northern Patagonia localities and
the Ovando River. TSA10.2, TSA10.3, TSA6.1, and
TSA17.1 haplotypes were found in a frequency ranging from
9.0 to 4.9 % in individuals distributed in northern and
444 Genetica (2012) 140:439–453
Table 1 GeneBank accession, haplotype name, and variable sites for the mtDNA control region sequences surveyed in Chinook salmon native and introduced populations
Accession no. or
Haplotype 203 383 408 649 650 745 779 986 1006a 1019 1021 1032 1033 1050 1081 1089 1099 1130 1134 1136 1139 1147
Shedlock et al. (1992) HapS G C G C C G G A G T C G C T T C A A C C G A
Nielsen et al. (1998) TSA1
???????.. .T........./-..
TSA2 ? ? ? ? ? ? ? . A . T . ..........
TSA3 ? ? ? ? ? ? ? . . . T . ...A......
TSA4 ? ? ? ? ? ? ? . . . T . .......A..
TSA5 ? ? ? ? ? ? ? . . . T . . . 81i
TSA6 ? ? ? ? ? ? ? . . . . . ..........
TSA7 ? ? ? ? ? ? ? . . . T . . G . A . .....
TSA8 ? ? ? ? ? ? ? . . . T . . G . . . .....
TSA9 ? ? ? ? ? ? ? . A A T . . G . . . .....
EU489727 TSA1a ? ? ? ? ? A . . . . T . ..........
EU489729 TSA1b ? ? ? ? ? A A . . . T . ..........
EU489735 TSA2a ? ? ? ? ? A . . A . T . ..........
EU489732 TSA4a ? ? ? ? ? A . . . . T . .......A..
EU489726 TSA10 ? ? ? ? ? A . . . . T . .......–..
EU489738 TSA11 ? ? ? ? ? A . . . . T . ......A..
EU489724 TSA12 ? ? ? ? ? A . . . . T . .......–..
EU489737 TSA13 ? ? ? ? ? A . . . . T . .......–A.
EU489725 TSA14 ? ? ? ? ? A . . . . T . ...A...–A.
EU489736 TSA15 ? ? ? ? ? A . . . . T . ...A...–..
EU489734 TSA16 ? ? ? ? ? A . . . . T . ....G....G
EU489730 TSA17 ? ? ? ? ? A A . . . T . .....C....
EU489739 TSA18 ? ? ? ? ? A A . . . T T .....C....
EU489731 TSA19 ? ? ? ? ? A A G . . T . .....C....
EU489728 TSA20 ? ? ? ? ? A A . . . T . ...A.C....
EU489733 TSA21 ? ? ? ? ? A A . . . T . T . . A . C ....
EF531713 SC1 ? ? ? ? ? ? ? . . . T . .......–..
EF531711 WA2 ? ? ? ? ? ? ? . . . . . .......–..
EF531712 WA1 ? ? ? ? ? ? ? . . . T . .......–..
JX975268 TSA10.1 . T . . . A . . . . T . ......../-..
JX975269 TSA10.2 . T A T T A . . . . T . ......../-..
JX975270 TSA1.03 . T . T T A . . . . T . ......../-..
JX975274 TSA14.1 . T . . . A . . . . T . ...A...–A.
JX975275 TSA15.1 . T . . . A . . . . T . ...A...–..
JX975276 TSA6.1 . T . . . A . . . . . . .......–..
Genetica (2012) 140:439–453 445
southern localities. Finally, haplotype TSA15.1 was repre-
sented in 2.8 % of the individuals and was recorded at the
Corcovado and Vargas Rivers (Table 3; Fig. 2).
Average non-native population gene diversity was higher
(h=0.656 ±0.109; excluding the Caterina River sample,
which was fixed for the TSA10.1 haplotype) than that
reported for the native Chinook salmon range [h=0.592 ±
0.070; excluding the Tucannon River sample, from the
Washington State, which was fixed for the TSA10 haplotype,
Table 2 Mean asymptotic values of four extrapolation estimators
and their confidence intervals (CI), where applicable, as applied to the
mtDNA Chinook salmon data
Hobs Chao
NA 17
Mean 18.25 25.00 24.98 21.86
95 % CI lower
16.27 17.52 NA NA
95 % CI upper
35.04 69.28 NA NA
NZ 5
Mean 5.00 5.00 3.81 6.18
95 % CI lower
5.00 5.00 NA NA
95 % CI upper
5.00 6.12 NA NA
Mean 5.00 5.00 6.25 5.35
95 % CI lower
5.00 5.00 NA NA
95 % CI upper
5.00 5.88 NA NA
NA North American samples, NZ New Zealand samples, PAT Pata-
gonia samples
0 50 100 150 200 250 300 350 400
Number of Haplotypes
Sampled individuals
Fig. 3 Rarefaction curves of observed haplotype diversity in mtDNA
data detected at each range: NA North America, NZ New Zealand,
and PAT Patagonia
Table 1 continued
Accession no. or
Haplotype 203 383 408 649 650 745 779 986 1006a 1019 1021 1032 1033 1050 1081 1089 1099 1130 1134 1136 1139 1147
JX975277 TSA17.1 . T . . . A A . . . T . .....C....
Nucleotide (nt) numbers corresponds to those given in Digby et al. (1992) for O. mykiss. The ‘‘–’’ represents a gap, ‘‘?’’ represents a missing nt and ‘‘.’’ matches the nucleotide in the first
TSA1 from Nielsen et al. (1998) is equivalent to CH1 and CH4 described in Nielsen et al. (1994), which differ by a base change at position 1,136 (a C in CH1 and a deletion in CH4)
An 81-base-pair insertion was found in Chinook salmon
446 Genetica (2012) 140:439–453
data from Martin et al. (2010)], but this difference was not
significant (one-tailed ttest =-0.625, P[0.05). However,
non-native populations exhibited a lower yet non-significant
(one-tailed ttest =0.172, P[0.05, Table 3) average
nucleotide diversity (p=0.0014 ±0.0007) than native
populations (p=0.0018 ±0.0007). In the introduced
range, increased genetic diversity was observed at rivers
close to or at original points of introduction, including the
Corcovado, Vargas, Cobarde, Prat, and Serrano Rivers,
ranging from 0.833 to 0.592, compared to less diverse
peripheral locations (Ovando and Caterina, h=0.436 and
0.000, respectively). The Pichicolo sample exhibited low
levels of genetic diversity, characteristic of hatchery stocks.
Nucleotide diversity followed the same trend (Table 2).
AMOVA analyses indicated that in the native region, 53.6 %
(P\0.0001) of the total genetic variation occurred among
populations, with the remainder within populations. In con-
trast, introduced populations in Patagonia exhibited lower
among population genetic variation (36.9 %, P\0.0001)
and higher within-population variation (64.1 %).
Despite higher within-population variation, significant
population subdivision was found among introduced Chinook
salmon populations in Chile and Argentina (U
P\0.001). In U
pairwise comparisons, the following three
population tests were non-significant: Cobarde versus Vargas,
Vargas versus Ovando, and Cobarde versus Ovando. In Co-
barde versus Ovando, the lack of U
significance might be due
to small sample size, whereas the remaining population-pairs
showed significant differentiation with U
values ranging
from 0.111 to 0.872 (P\0.017) (Table 4). The most note-
worthy significant pairwise U
comparisons involved the
Serrano and Caterina samples. As expected from these results, a
relationship between population differentiation and geograph-
ical distance among introduced populations was not evident
(r =0.053, P[0.05), providing no foundation for IBD.
The combined use of historical and mitochondrial DNA
data enables the portrayal of inferences regarding the ori-
gins and colonization processes of Chinook salmon intro-
duced into Patagonian basins (41°–54°S). Our results also
support the hypothesis that multiple introductions resulted
in the establishment of genetically diverse populations.
Moreover, we found evidence for admixture and geneti-
cally novel combinations in several sampled locales. His-
torical records suggest that Chinook salmon have been
repeatedly and intensively introduced to several locations
in Chile for at least 30 years, and from as many as six
geographically distinct Chinook origins, from the follow-
ing stocks: Washington State, including the Cowlitz River
Fig. 4 MDS plot based on the Manhattan distance constructed from
mtDNA haplotype frequencies for Chinook salmon populations from
the native, New Zealand, and introduced ranges. Population similarity
is indicated by gray-scale shading. Populations codes are: Native
range: Kam: Kamchatka, RU; Yuk: Yukon, AK; Tul: Tuluksak, AK;
Gul: Gulkana, AK; Chi: Chilliwack River, BC; UWa: University of
Washington, WA; Pri: Priest Rapids, WA; Lyo: Lyons Ferry, WA;
Tuc: Tucannon, WA; Wil: Willamette River, OR; Ame: American
River, CA; Tuo: Tuolumne River, CA; and Sac: Sacramento River,
CA. New Zealand: Clu: Clutha River, NZ; Wai: Waitaki River, NZ;
Rak: Rakaia River, NZ; and Wam: Waimakariri, NZ. Introduced
range (Patagonia): Cob: Cobarde River, CH; Cor: Corcovado River,
AR; Var: Vargas River, CH; Ser: Serrano River, CH; Pra: Prat River,
CH; and Cat: Caterina River, AR
Fig. 5 Ninety-five percent statistical parsimony haplotype network
for Chinook salmon based on mtDNA control region short haplotypes
(414-bp). Circle size is proportional to the number of individuals.
Each line represents a single mutation; black dots represent inferred
non-sampled or extinct haplotypes
Genetica (2012) 140:439–453 447
Table 3 Descriptive statistics of mitochondrial DNA (mtDNA) control region comparing genetic variation among Chinook salmon populations from introduced and native ranges
Locality n20 21 16 19 18 17 1B 1A 10 11 13 12 14 4A 2A 15 6 H HpReferences
1. Kamchatka, RU 31 1 1 28 1 4 0.187
Martin et al.
2. Yukon, AK 20 2 9 9 3 0.616
Martin et al.
3. Tuluksak, AK 26 5 1 12 8 4 0.680
Martin et al.
4. Gulkana, AK 22 2 20 2 0.173
Martin et al.
5. Chilliwack River, BC 23 3 3 15 1 1 5 0.561
Martin et al.
6. University of Washington
(Kalama River), WA
32 32 11 2 n.p. n.p. Becker et al.
7. Priest Rapids, WA 22 1 9 2 4 6 5 0.749
Martin et al.
8. Lyons Ferry, WA 22 1 1 1 11 3 4 1 7 0.723
Martin et al.
9. Tucannon, WA 21 21 1 0 0 Martin et al.
10. Willamette River, OR 24 2 8 7 7 4 0.743
Martin et al.
11. American River, CA 27 8 11 3 4 1 5 0.738
Martin et al.
12. Tuolumne River, CA 23 2 9 7 4 1 5 0.747
Martin et al.
13. Sacramento River, CA
(fall run)
75 20 16 21 8 10 5 n.p. n.p. Williamson and
May, (2007)
14. Clutha River, NZ 62 51
11 0 4 n.p. n.p. Quinn et al.
15. Waitaki River, NZ 34 26
7 1 4 n.p. n.p. Quinn et al.
16. Rakaia River, NZ 37 30
1 6 4 n.p. n.p. Quinn et al.
17. Waimakariri, NZ 39 34
3 1 1 5 n.p. n.p. Quinn et al.
448 Genetica (2012) 140:439–453
Table 3 continued
Locality n20 21 16 19 18 17 1B 1A 10 11 13 12 14 4A 2A 15 6 H HpReferences
18. Cobarde River, CH 22 1 12
3 1 6 0.636
This study
19. Corcovado River, AR 4 1
2 1 3 0.833
This study
20. Vargas River, CH 25 5 8
7 3 6 0.793
This study
21. Serrano River, CH 16 1
3 0.592
This study
22. Prat River, CH 21 8 10
2 4 0.647
This study
23. Caterina River, AR 20 20
1 0 0 This study
24. Ovando River, AR 8 2
6 2 0.436
This study
25. Pichicolo Hatchery, CH 25 21
4 2 0.280
This study
n, number of samples; H, number of haplotypes, h(SD), gene diversity and its standard deviation, p(SD), nucleotide diversity and its standard deviation, n.p., analysis not performed. For
haplotype TSA10 the superscript indicates the longer haplotype type. Localities: RU, Russia; AK, Alaska; BC, British Columbia; WA, Washington; OR, Oregon; CA, California; NZ, New
Zealand; CH, Chile and AR, Argentina. Haplotype information for Russia, Alaska, British Columbia, Washington, Oregon and California based on Martin et al. (2010) (414-bp); for the
Sacramento River based on Williamson and May (2007) (237-bp) and for New Zealand based on Quinn et al. (1996) (170-bp)
In Quinn et al. (1996) the base change differentiating haplotypes TSA1a and TSA10 (CH1 and CH4, respectively, in that study) was difficult to score consistently in the NZ fish, therefore they
pooled mtDNA types 1 and 4
Genetica (2012) 140:439–453 449
(introduced from 1978 to 1983), UW (1982–1989), and the
Puget Sound (1987–1997); populations from Oregon
(1987–1988); British Columbia; and New Zealand (intro-
duced from 1988 to 2000). The mtDNA data largely cor-
roborated historical records, detecting a close affinity
among Chinook salmon stocks from the University of
Washington and British Columbia (TSA10, TSA6 and
TSA17) and the Cobarde, Prat, Caterina and Serrano
populations, whereas closest genetic affinities were detec-
ted among Oregon (TSA14), and to a lesser extent, New
Zealand (TSA15) with the Vargas, Ovando and Corcovado
Rivers populations. Previous studies based on historical
records and field data alone contended that naturalized
populations of Chinook salmon in Patagonia were likely
derived from ocean ranching operations in Chile (Correa
and Gross 2008). However, our results indicate that
invading Chinook salmon have likely originated from both
early ocean ranching and recent net pen operations in
Genetic patterns observed in introduced populations that
exhibited haplotypes with distantly disjunct distributions in
the native range co-occur in Patagonia. This is congruent
with the hypothesis that introduced populations have
multiple source origins. Moreover, at least four of the
seven introduced populations sampled in this study (Co-
barde, Corcovado, Vargas, and Prat) exhibited haplotypes
that originated from more than one distinct native source,
reflecting genetic mixing from previously isolated lineages.
For example, haplotypes sampled from Chilean locations
north of 47°S (TSA6, 10, 14, 15, and 17) suggested
ancestral contributions from all putative stocks, whereas
the Prat River haplotype composition (TSA6, 10, and 17)
indicated ancestral contributions derived from fewer sour-
ces, primarily the Washington State. When we consider
historical records, we cannot rule out secondary coloniza-
tion from additional sources introduced at Curaco de Ve
such as British Columbia. Due to the overall absence of
genetic diversity, molecular data were not useful to clarify
Chinook salmon origins in the Caterina River. However,
historical data (reports of first sightings soon after the
initiation of the ranching experiments on the Prat River)
lead to support the hypothesis proposed by Ciancio et al.
(2005) that the invasion was likely the result of imports
into southern Chile in the early 1980s.
As expected from admixture following multiple intro-
duction events, genetic diversity in the non-native Chinook
salmon populations sampled in this study was not signifi-
cantly lower than in native source populations, despite a
trend towards slightly lower nucleotide variation. Increased
genetic diversity in introduced relative to native popula-
tions have been also observed in invading populations of
brown anole lizards Anolis sagrei (Kolbe et al. 2004) and
of the amphipod Gammarus tigrinus (Kelly et al. 2006).
Both studies suggested that interbreeding among individ-
uals from different native-range sources caused admixture,
which combined among-population genetic variation from
multiple genetically differentiated sources to increase
genetic variation within introduced populations. The
notable loss of genetic diversity in the Caterina River
Chinook salmon, however, might result from the interac-
tion between recent (secondary) founder events, which are
typical in populations founded from noncontiguous colo-
nization at the extreme edge of an invasion range (Hewitt
1996; Ibrahim et al. 1996), and rapid selection due to
strong local adaptation in this population.
Significant population differentiation, but no evidence
of IBD or a geographic cline, was observed within our
study area, which is to be expected if the invasion expan-
ded gradually in a front-like manner, whereby the most
recently invaded location was the source of further inva-
sion. In most cases, genetic distances were low and pop-
ulations diverged less than would be expected for the
distance separating each population. This pattern can be
better explained by the introduction of the same Chinook
salmon genetic sources to different locations in the invaded
range than by progressive expansion and contiguous dis-
persal. The exception was the Serrano River, which
exhibited more genetic divergence than expected, even
from the nearby Prat River, located a short geographic
distance away (60 km). The two locations are situated
Table 4 Results of pairwise comparisons of non-native Chinook salmon populations in Chile and Argentina
Cobarde Vargas Serrano Prat Caterina Ovando
Cobarde – 610 1,020 960 2,670 1,525
Vargas 0.057 610 550 1,525 1,115
Serrano 0.442*0.531* – 60 1,035 625
Prat 0.160*0.106*0.597** – 975 565
Caterina 0.111*0.196** 0.852** 0.462* – 860
Ovando 0.319 0.109 0.791*0.359*0.872*–
values are given below the diagonal and the geographic distances between river mouths (km) above the diagonal. Bold tests and levels of
significance after false discovery rate correction (a=0.003) are marked with * PB0.05 and ** PB0.01
450 Genetica (2012) 140:439–453
within the U
´ltima Esperanza Sound, an inland waterway
that empties the Cordillera del Paine. Although hydrolog-
ical studies have documented a significant net outflow of
surface waters, local bathymetry creates a relatively high
retention time, which may hamper the exchange between
marine and freshwater fauna (Antezana 1999) and explain
low Chinook salmon dispersal (particularly smolts) in and
out of the Sound. The markedly high levels of genetic
differentiation in the Caterina River, the most remote
location, suggest that this population arose via geographic
isolation and is currently disconnected from the remaining
colonizing populations (but see above also for alternative
We also detected several instances of long distance
southward dispersal. For example, haplotype TSA15,
introduced from New Zealand to northern Chilean localities
(42°S) in the 1990s, was first recorded in the Vargas River
in the year 2000, 700 km south of the introduction sites. The
presence of haplotypes TSA14 (derived from Oregon) and
TSA10.3 (unknown ancestry) in the Ovando and Serrano
Rivers, which appear in high frequencies at northern Chil-
ean locales ([1,100 km for the Ovando population) but are
absent in the geographically closer Prat population (Fig. 2),
is consistent with a hypothesis of a general pattern of
southern spread by noncontiguous dispersal.
These results are also congruent with the ocean circu-
lation patterns around southern South America, largely
dominated by the cold waters of the westward flowing
West Wind Drift, and the southward flowing Cape Horn
Current, which would facilitate southward salmon dispersal
from Chilean locations into Antarctic convergence waters
and further into the Patagonian Shelf in the southwestern
Atlantic Ocean (Becker et al. 2007). Other authors have
proposed a similar dispersal scenario for rockfishes along
the coast of South America via the Humboldt Current and
the West Wind Drift current (Eschmeyer and Hureau 1971;
˜ez et al. 2010). As net pen Chinook salmon cultures in
Chile moved further south and occupied new watersheds,
the risk of exotic Chinook salmon spreading further and
colonizing aquaculture-free Patagonian basins, is extre-
mely high (Consuegra et al. 2011; Ferna
´ndez et al. 2010;
Pascual et al. 2009).
In conclusion, our study indicates that the deliberate
introduction of Chinook salmon from several founding
sources into Patagonia has contributed to the maintenance
of high levels of genetic variation within non-native popu-
lations, thus avoiding the loss of genetic variation associ-
ated with the colonization of new habitats. These high levels
of genetic variation may have facilitated the successful
establishment of Chinook salmon populations in Patagonia.
Acknowledgments This research was supported by grants from the
Agencia Nacional para la Promocio
´n de la Ciencia y la Tecnologı
Argentina to M. Pascual; the Universidad de Concepcio
´n, Chile to B.
Ernst-Elizalde; and the Universidad Austral, Chile to E. Aedo Mar-
chant. Sincere thanks to personnel of Centro Trapananda, Universidad
Austral, Chile for their help during specimen collection, to N. Bou-
stead and M. Unwin, National Institute for Water and Atmospheric
Research Ltd., New Zealand for providing specimens for analysis,
and L. Real and P. Quiroga, Centro Nacional Patago
´nico, CONICET,
Argentina for assistance with laboratory analyses and figure maps,
respectively. We are indebted to Mr. K. Martin, Dr. G. Thoorgaard,
and Dr. Shedlock for providing sequence data and phylogenetic
information. The authors are very grateful to the editor for spending
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Supplementary resources (10)

... The earliest attempts to introduce Chinook salmon, Oncorhynchus tshawytscha (Walbaum), in Chile date back to the years 1886, 1924, and 1930, but the efforts were unsuccessful (Riva Rossi et al., 2012). Later, Chinook salmon were introduced into Chile for sport fishing and aquaculture purposes during the 1970s (Soto et al., 2007;Di Prinzio et al., 2015). ...
... Later, Chinook salmon were introduced into Chile for sport fishing and aquaculture purposes during the 1970s (Soto et al., 2007;Di Prinzio et al., 2015). Riva Rossi et al. (2012) concluded that the invasion of Chinook salmon occurred between 39°S and 56°S latitude and arose from populations originating in northwest North America and New Zealand based on genetic data (Riva Rossi et al., 2012). The establishment of Chinook salmon in both Argentinean and Chilean rivers in the late 1970s had its probable origin in the escape of introduced fish from farming centers and ranching programs in Chile (Riva Rossi et al., 2012;Di Prinzio et al., 2015). ...
... Later, Chinook salmon were introduced into Chile for sport fishing and aquaculture purposes during the 1970s (Soto et al., 2007;Di Prinzio et al., 2015). Riva Rossi et al. (2012) concluded that the invasion of Chinook salmon occurred between 39°S and 56°S latitude and arose from populations originating in northwest North America and New Zealand based on genetic data (Riva Rossi et al., 2012). The establishment of Chinook salmon in both Argentinean and Chilean rivers in the late 1970s had its probable origin in the escape of introduced fish from farming centers and ranching programs in Chile (Riva Rossi et al., 2012;Di Prinzio et al., 2015). ...
In the present study, the zoonotic tapeworms Dibothriocephalus latus and Dibothriocephalus dendriticus were identified for the first time, using morphological and molecular procedures, in a population of introduced Chinook salmon in Chile. The morphological differences observed between plerocercoids of D. latus and D. dendriticus were, respectively, a retracted and obscured scolex versus one that is always visible and only partially retracted after cold fixation; extension of frontal glands; size, types of, density of, and distribution of microtriches; and number of parenchymal longitudinal muscle bundles within 50-m spaces. With scanning electronic microscopy, both species presented 3 types of microtriches: coniform and uncinated spinitriches, and capilliform filitriches. In the body region, D. latus presents all types of microtriches, but D. dendriticus only possessed capilliform filitriches. Multiplex PCR targeting cox1 of Diphyllobothriidae and subsequent sequence analysis allowed for confirmation of species identity. All adult Chinook salmon examined (3260 cm total length) were infected by Dibothriocephalus spp. with a range of 15192 plerocercoids. Plerocercoids were found in the stomach, intestine, liver, spleen, gonads, swim bladder, peritoneum, heart, and muscles. The prevalence of infected salmon, the percentage of plerocercoids, and the mean intensity of D. latus in the muscles were 3, 4, and 2 times greater than that of D. dendriticus. Histological examination of the stomach, liver, spleen, gonads, and muscle revealed the presence of 1 or more encysted or free plerocercoids. In most cases, varying degrees of chronic inflammation and low presence of neutrophils were observed. The prey consumed by Chinook salmon included the native fish, Galaxias maculatus, and unidentified fish and amphipods. Other identified endohelminths were Derogenes lacustris Tsuchida, Flores, Viozzi, Rauque, and Urabe, 2021 in the stomach, Camallanus corderoi Torres, Teuber and Miranda, 1990 in the intestine, larvae of Contracaecum sp. in the intestinal wall, and Acanthocephalus tumescens (von Linstow, 1896) in the intestine. All identified parasites are reported for the first time in Chinook salmon from Chile.
... Our study is distinguished from previous molecular studies of Patagonian Chinook salmon 18,19,[23][24][25] in three principal ways: (1) We used the most inclusive baseline dataset possible, including all potential North American donor lineages. Previous studies have been more or less limited by the number of reference lineages available for particular genetic markers. ...
... Initially, we assumed high genetic diversity, i.e., heterozygosity and allelic richness, was a result of mixed ancestry. Previous studies have made similar conclusions 18,19,24 . CML mixture analysis and M-BC both estimated more founding lineages in the two northern Patagonian sites. ...
... Previous studies have inferred ancestral affiliation from the University of Washington Hatchery based on mitochondrial DNA 23,24 , but owing to the low resolution of those analyses (incomplete baselines; geographically wide-spread haplotypes), those results deserve further scrutiny. Other investigators, using SNPs and a more extensive baseline 31 , found little evidence to support South Puget Sound ancestry, although they still suggested a possible contribution of University of Washington Hatchery stock based on its supposed origin from lower Columbia River lineages, which do appear as major contributors to Patagonian populations 18,19 . ...
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Chinook salmon native to North America are spreading through South America’s Patagonia and have become the most widespread anadromous salmon invasion ever documented. To better understand the colonization history and role that genetic diversity might have played in the founding and radiation of these new populations, we characterized ancestry and genetic diversity across latitude (39-48°S). Samples from four distant basins in Chile were genotyped for 13 microsatellite loci, and allocated, through probabilistic mixture models, to 148 potential donor populations in North America representing 46 distinct genetic lineages. Patagonian Chinook salmon clearly had a diverse and heterogeneous ancestry. Lineages from the Lower Columbia River were introduced for salmon open-ocean ranching in the late 1970s and 1980s, and were prevalent south of 43°S. In the north, however, a diverse assembly of lineages was found, associated with net-pen aquaculture during the 1990s. Finally, we showed that possible lineage admixture in the introduced range can confound allocations inferred from mixture models, a caveat previously overlooked in studies of this kind. While we documented high genetic and lineage diversity in expanding Patagonian populations, the degree to which diversity drives adaptive potential remains unclear. Our new understanding of diversity across latitude will guide future research.
... In this study we recovered high genetic divergence between Geotria west and east to the Andes, meanwhile in Argentina, populations spanning across the extra-Andean Patagonian steppe were almost monomorphic, with negligible levels of genetic structuring, a pattern concordant with the phylogeographic patterns documented in several freshwater species of Patagonia [71,[75][76][77][78]. Several South American freshwater fish species display deep phylogeographical differences that likely represent the split of Atlantic and Pacific lineages and have been associated with the uplift of the southern Andes (beginning 23 million years ago) and the Table 2. Results of ABGD analyses with the Jukes-Cantor (JC69), Kimura (K80), and the uncorrected p-distance (SD) models for the two data sets. ...
... However, on the east side of the Andes, fish species from Atlantic drainages exhibit low phylogeographic structure and divergence [71,[75][76][77][78]. This is consistent with our results indicating that populations of Geotria from Argentina spanning across the extra-Andean Patagonian steppe were almost monomorphic, with negligible levels of genetic structuring. ...
... Such movements are favored by the cold waters of the eastward flowing West Wind Drift and southward by the Cape Horn Current and the Antarctic Circumpolar Current to continue eastward and northward converging into the Malvinas (Falkland) Current (Fig 8). This facilitates southward salmon dispersal from Chilean locations into the Antarctic convergence and into the Patagonian Shelf in the southwestern Atlantic Ocean [74,75]. ...
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Background The Argentinian pouched lamprey, classified as Petromyzon macrostomus Burmeister, 1868 was first described in 1867 in De La Plata River, in Buenos Aires, Argentina, and subsequently recorded in several rivers from Patagonia. Since its original description, the validity of P. macrostomus was questioned by several ichthyologists and 36 years after its original discovery it was considered a junior synonym of Geotria australis Gray, 1851. For a long time, the taxonomic status of G. australis has been uncertain, largely due to the misinterpretations of the morphological alterations that occur during sexual maturation, including the arrangement of teeth, size and position of fins and cloaca, and the development of an exceptionally large gular pouch in males. In this study, the taxonomic status of Geotria from across the “species” range was evaluated using both molecular analysis and examination of morphological characteristics. Methodology/principal findings Phylogenetic and species delimitation analyses based on mitochondrial DNA sequences of Cytochrome b (Cyt b) and Cytochrome C Oxidase Subunit 1 (COI) genes, along with morphological analysis of diagnostic characters reported in the original descriptions of the species were used to assess genetic and morphological variation within Geotria and to determine the specific status of the Argentinian lamprey. These analyses revealed that Geotria from Argentina constitutes a well differentiated lineage from Chilean and Australasian populations. The position of the cloaca and the distance between the second dorsal and caudal fins in sub-adult individuals, and at previous life stages, can be used to distinguish between the two species. In addition, the genetic distance between G. macrostoma and G. australis for the COI and Cyt b mitochondrial genes is higher than both intra- and inter-specific distances reported for other Petromyzontiformes. Conclusions/significance Our results indicate that the Argentinian pouched lamprey, found along a broad latitudinal gradient on the south-west Atlantic coast of South America, should be named as Geotria macrostoma (Burmeister, 1868) and not as G. australis Gray 1851, returning to its earliest valid designation in Argentina. Geotria macrostoma can now be considered as the single lamprey species inhabiting Argentinian Patagonia, with distinct local adaptations and evolutionary potential. It is essential that this distinctiveness is recognized in order to guide future conservation and management actions against imminent threats posed by human actions in the major basins of Patagonia.
... Chinook salmon and rainbow trout were successfully introduced and established naturalized populations across Patagonia (Arismendi et al., 2014;Correa and Gross, 2008;Riva-Rossi et al., 2012). Both species have contributed to local economies due to their value for recreational fisheries (Arismendi and Nahuelhual, 2007), and more recently, artisanal fisheries in the case of Chinook salmon (Sanguinetti et al., 2021). ...
... We assert that implementing fatty acid analyses is an appropriate methodological tool for assessing ecological interactions, in our case, transfer of key MDN from anadromous to resident invasive salmonids, and thus contributing to holistic management and decision-making strategies on multiple invaders. Because our results emanate from a study on one basin, we encourage future studies to consider multiple sites across the range of invaded ecosystems and basins draining to both Pacific Ocean (Arismendi et al., 2014;Correa and Gross, 2008;Musleh et al., 2020) and Atlantic Ocean (Fernández et al., 2010;Nardi et al., 2019;Riva-Rossi et al., 2012) in South America. ...
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Marine derived nutrients (MDN) contained in gametes (mature eggs and sperm), carcasses and metabolic wastes from anadromous migratory salmon can transfer energy and materials to fresh water, thereby affecting the structure and function of stream ecosystems. This is crucial among ecosystems where humans have mediated biological invasions by propagating non-native species. Previous studies have demonstrated that consumption of MDN from salmon can benefit both native and invasive resident fishes. Yet, a more detailed understanding of the transfer of biomolecules with important physiological functions such as ω-3 highly unsaturated fatty acids (HUFAs) have received less attention among researchers. Here we demonstrate that consumption of MDN contained in invasive Chinook salmon eggs transfers ω-3 HUFAs (e.g., EPA and DHA) to resident invasive rainbow trout in a river food web. We conducted a field study in river sections previously identified as spawning areas for Chinook salmon in the Cisnes River, Patagonia. Rainbow trout were sampled around salmon spawning areas before, during, and after the salmon spawning season. Additionally, we collected tissue from different food resources and components of different origin (e.g., primary producers, aquatic and terrestrial items) from Cisnes River system. Analyses of stomach contents of trout were performed in conjunction with analyses of both lipid content and fatty acid profiles of trout tissue and food web components. Chinook salmon eggs showed higher content of ω-3 HUFAs, especially EPA (31.08 ± 23.08 mg g DW-1) and DHA (27.50 ± 14.11 mg g DW-1) than either freshwater or terrestrial components (0-6.10 mg g DW-1 both EPA and DHA). We measured marked shifts in the fatty acid profile (~six-fold increase in EPA and DHA) of trout following consumption of Chinook salmon eggs. Our findings suggest that MDN via consumption of salmon eggs by resident rainbow trout may positively influence resident trout and likely contribute to gauge synergistic interactions between invaders on receiving ecosystems of Patagonia region.
... farmed species during the past 20 years 25 there are no reports of selfsustaining populations; some authors have argued that this species could be less adapted to colonize environments in the Southern Hemisphere. Comparison has been made with the invasion success of Chinook salmon in southern Chile and Argentina which, interestingly has not been generated by massive escapes, but rather by several sparse events and thus the successful colonization has been probably due to the ability of the species to colonize new habitats.8,74,75 Nevertheless, there is no guarantee that continuing escapees of Atlantic salmon,F I G U R E 4 (a) Sensitivity index per relevant water body (RWB; n = 20) for Atlantic salmon. ...
Here, we review extensive information to estimate environmental risks from escaped non‐native salmonids based on the assessments of hazard, sensitivity and exposure of discrete water bodies in Chile. In 2020, the country harvested about 1 million tons salmonids from net pens located along 1500 km of highly biodiverse coastline. We base our analysis on existing scientific information and authors' expert opinions including an assessment of knowledge gaps and uncertainties. Risks of environmental impacts differed by salmon species, being lowest for Atlantic salmon due to its estimated lower survival, lower ability to feed after escaping and lower reproductive capacity in the wild compared to coho salmon and rainbow trout. Overall risks due to escapes of any of the species were highest in areas of both high farming intensity and low capacity of mitigating escapes (by wild predators and fishers) such as Aysén District. At same time, risk was higher in the most farmed areas that also presented suitable habitats to support reproduction and juvenile salmonid rearing. However, the risk estimation certainty differed among species being lowest for Atlantic salmon due to insufficient monitoring of their fate in the wild. Monitoring the fate and impacts of escaped salmonids, specially in higher risk areas is recommended to improve risk projections and to prevent and mitigate further impacts. Since Atlantic and coho salmon are not yet successful invaders in Chile, research attention is urgently needed to assess the environmental consequences of escapes of these species. The present approach can be applied to any aquaculture system given the availability of information on farmed species and receiving ecosystems.
... Otro de los impactos negativos en los ecosistemas de la región derivado de esta industria ha sido el escape de salmones desde las granjas al medio natural, donde alteran los ecosistemas naturales al depredar especies nativas y competir por alimento con ellas . Prácticamente no hay lugar en la Patagonia que se encuentre a salvo de la colonización futura de estas especies, ya que en años recientes se ha documentado un continuo incremento en su distribución en la región (Figura 18); (Becker et al ., 2007;Fernández et al ., 2010;Riva Rossi et al ., 2012) . La dieta de los salmones escapados incluye peces, crustáceos, insectos y moluscos (Soto et al . ...
Technical Report
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Informe de las Expediciones de National Geographic Pristine Seas y Comunidades Kawésqar y Yagán.
... The clear fishery potential of Chinook salmon triggered government-sponsored and private initiatives to propagate it throughout Pacific Ocean watersheds in South America during 1978-1990(Correa and Gross 2008, with donor (native) populations spanning multiple geographic regions from North America (Correa and Moran 2017;Gomez-Uchida et al. 2018;Riva Rossi et al. 2012). These introduction efforts failed to yield a sustainable commercial activity, but resulted in the naturalization of multiple populations. ...
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Invasive species with migratory behavior and complex life cycles represent a challenge for evaluating natal sites among individuals. Private and government-sponsored initiatives resulted in the successful introduction and naturalization of Chinook salmon (Oncorhynchus tshawytscha) throughout northern and southern Patagonia in South America. Migratory populations of Chinook salmon breed in fresh water, but spend most of their life feeding at sea, forming abundant populations in several watersheds draining into the southeast Pacific Ocean. We used single nucleotide polymorphisms combined with genetic structure and mixed-stock analyses to evaluate natal sites of Chinook salmon at sea caught in one estuary and two coastal locations compared to reference populations from breeding sites in fresh water. Firstly, Bayesian individual-assignment analyses revealed no genetic structure among adults caught off the coast of the Toltén River and migrating (maturing) adults caught in Toltén River estuary, suggesting they likely belong to a single population. Secondly, mixed-stock genetic analyses revealed that most Chinook salmon caught in one estuary and two coastal locations likely originated from spawners from the nearest river (86–96%). Contributions from distant watersheds to mixtures at sea decreased with increasing geographic distance. Our combined genetic evidence points strongly to homing among non-native Chinook salmon, whereby most adults return to breed to their natal river amid potentially long-distance migrations through the coast. Mixed-stock genetic analyses provide considerable potential to identify the population of origin of Chinook salmon mixtures caught off the coast. They also seem an appropriate proof of concept to assess homing versus dispersal and infer invasion pathways via long-distance migration.
The Patagonian steppe is a vast territory with a diverse array of aquatic environments with low fish richness, including several exotic species which are mostly salmonids. Unlike the Andean region, knowledge of the ichthyofauna and fisheries of the Patagonian plateau is comparatively scarce. The characteristics of the ichthyofauna and their assemblages and fisheries vary greatly in the large basins that cross the steppe. Fish assemblages of north Patagonia include elements of the Patagonian, Andean Cuyean, and Pampean ichthyological provinces, where Austral and Brazilic subregion species overlap. Salmonid richness increases from northern to southern latitudes, as do anadromous species. The steppe also presents some endorheic basins inhabited by species of high conservation value and restricted distribution. Threats and impacts that have been identified include land and water use, damming, pollution, climate change, and exotic species introduction. Historical and current management policies have permitted uncontrolled stocking of exotic species due to their high fishing value, thus favoring a reduction in the distribution and abundance of native fishes, including endangered species with an extreme degree of endemism.KeywordsPatagonian steppeNon-native speciesNative speciesManagement policiesSalmonid introductionsSalmonid impactFish assemblageRecreational and artisanal fisheries
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The present study is a full review of the non-native freshwater fish species introduced into Argentina and their relationship to the main environmental features and introduction vectors of each freshwater ecoregion. The total number of non-native freshwater fish species was compiled through a literature survey; information on spatial–temporal patterns of species records and invasion vectors was retrieved for all ten freshwater ecoregions of Argentina. Our survey revealed that 18–22 non-native fish species had been recorded up to 1999, and a total of 40 introduced fish species, of which 18 are invasive and five potentially invasive, had been registered in seven Argentinean ecoregions as of May 2020. According to georeferenced records, the rainbow trout Oncorhynchus mykiss and common carp Cyprinus carpio were the non-native fish species with the greatest number of records and largest invaded areas, probably due to their species-specific ecological traits. Invasive fish species differed clearly between the Patagonia, Lower Paraná, and Lower Uruguay ecoregions, probably because of a combination of the environmental conditions, structure of native assemblages, and invasion pathways in each ecoregion. Except for the recognized impact of non-native salmonids, the adverse effects of introduced fish species have been little studied, indicating the need for further research to clarify the role of ecological shifts triggered by the introduction and establishment of non-native fish species in Argentina. In contrast to the high diversity of aquatic species and freshwater environments, the spread and impact of invasive fish species in Argentina is little known, particularly compared with other South American countries.
Les invasions biologiques sont une composante majeure des changements globaux, causant de nombreuses perturbations dans le fonctionnement des écosystèmes et les activités humaines. Leur fréquence augmente depuis la fin du XXème siècle, notamment dans le cas des champignons pathogènes des arbres forestiers. Dans ce contexte d'introduction, l’adaptation des agents pathogènes à de nouveaux environnements et de nouveaux hôtes constitue un paradoxe évolutif, du fait d'une faible diversité génétique généralement introduite. Des mécanismes évolutifs permettant l’adaptation de ces organismes ont été proposés, mais à l’exception de quelques espèces modèles, souvent agents pathogènes de plantes cultivées, ces mécanismes restent peu étudiés chez les champignons.Cette thèse a pour but d’étudier l’évolution des populations de Cryphonectria parasitica, l’agent causal du chancre du châtaignier, dans le contexte d’une double introduction en Europe. Originaire d’Asie, il a été introduit en Amérique du Nord à la fin du XIXème siècle, entraînant la disparition quasi-totale des populations naturelles de châtaigniers américains. Il a ensuite été introduit en Europe depuis ces populations nord-américaines et des populations asiatiques au début du XXème siècle. En Europe, les populations sont majoritairement structurées en lignées clonales contrairement aux populations d’origine. Ceci suggère un changement de mode de reproduction pouvant être impliqué dans le succès invasif de ces populations. Pourtant, les études précédentes ont montré que plusieurs génotypes n’appartenant pas aux principales lignées clonales se sont maintenus lors de la colonisation et que des croisements entre ces lignées clonales existent, même s’ils semblent limités. Les objectifs de cette thèse ont été de mieux décrire les croisements entre les lignées clonales et d’identifier de possibles barrières aux croisements entre celles-ci.Dans une première partie, le génome de 50 isolats français, nord-américains et asiatiques ont permis de confirmer la forte similarité des isolats appartenant à une même lignée clonale européenne, à l’exception de petites régions divergentes échangées entre ces génomes, plus fréquemment observées entre lignées introduites d’une même origine. Par ailleurs, 5 des 6 lignées étudiées portent une signature d’échange récent de la région portant le gène du type sexuel, conférant aux lignées clonales la capacité de s’autoféconder (haploid-selfing). Ces résultats soulignent que le maintien de lignées clonales chez un champignon hétérothallique comme C. parasitica (cad que les croisements impliquent des génotypes avec des types sexuels différents) n’implique pas toujours et uniquement la reproduction asexuée.Dans une seconde partie, l’assemblage de génomes d’isolats provenant des aires d’origine et introduites, utilisant des méthodes de séquençage long brin, a permis de comparer leur structure et composition chromosomique, et d’identifier de possibles barrières à la recombinaison. Aucun réarrangement majeur n’a cependant été détecté à l’exception d’une région d’1Mb, adjacente au locus du type sexuel, très riche en éléments transposables et variable entre les génomes. Ces résultats semblent infirmer l’hypothèse d’isolement reproducteur par réarrangement du génome. En revanche, les zones contenant de nombreux éléments mobiles pourraient permettre une évolution rapide de C. parasitica lors de l’introduction.Une dernière partie aborde l’étude des génotypes semblant provenir de croisements entre les lignées clonales majoritaires afin d’explorer les processus de recombinaisons entre les pools génétiques des deux introductions et d’identifier de possible barrières à l’hybridation potentiellement associées à des combinaisons génétiques défavorables.Ce travail souligne l'apport des données génomiques dans la compréhension des processus de recombinaison et la détection des variations génétiques d'un champignon pathogène invasif affectant ses capacités évolutives.
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Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multilocus genotypes. A Windows version of the software is freely available on
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Hydrographic features and bottom profiles along the main passages from Paso Ancho in the Straits of Magellan to the Beagle Channel and those of adjacent oceanic waters are examined with regard to water origin and circulation. Sills and shallow entrances likely limited water exchange. Adjacent oceanic waters were warmest in the Atlantic and saltiest in the Pacific sectors. Waters within the inland passages were fresher and cooler than open shelf waters, showing a decreasing salinity gradient between the Beagle Channel and the Straits of Magellan and a subsurface wedge of warmest and saltiest oceanic water underneath a core of cold and brackish water in Brazo Noroeste. Subsurface water masses of the Straits of Magellan and Brazo Noroeste seem to be entrapped. Temperature and density distributions suggest that the inflow of salty and warm Pacific waters takes place through Bahia Cook. Westward and northward toward the Straits of Magellan, these waters may progressively mix with cooler and more brackish waters adjacent to Cordillera de Darwin. In this sector (Canal Brecknock-Canal Cockburn) stratification of the water column was weaker and became zero toward the Straits of Magellan (Seno Magdalena/Paso Ancho). Distribution of water properties was consistent with bathymetry profiles and suggests the following subdivision of microbasins along the Magellan-Beagle passage: 1.- Paso Ancho-Seno Magdalena, 2.- Canal Magdalena-Canal Brecknock, 3.- Canal Ballenero-Brazo Noroeste, 4.- Beagle Channel.
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One way to summarize the evolutionary dynamics of species introductions is to estimate how levels of genetic diversity in non-native populations are dif- ferent from those of their source populations. While it is typically assumed that a significant loss of diversity will be associated with species introduc- tions, the actual effect may be more complex, depending on propagule pressure and patterns of diversity and population structure in the native range of a species. We review a number of studies of animal species introductions in which allelic diversity and heterozygosity in the non-native and source ranges of each species can be compared, and find that the typical loss of diversity is minimal. The generality of this pattern may provide new insight into debates over the prevalence of stochastic processes in generating novel phenotypes or coadapted gene complexes in founder populations. These results suggest that the response of founder populations to natural selection in a novel environ- ment is generally more important than the stochastic effects of the founder event itself in determining the evolutionary trajectory of a population.
Genetic differentiation and species boundaries between Atlantic and Pacific lineages of the Patagonian rockfish Sebastes oculatus was investigated using mtDNA D-loop partial sequences (541 bp). Sequences were obtained for 47 individuals from seven locations off the Pacific and Atlantic coasts of South America (S. oculatus) and one off the coast of South Africa (S. capensis), and for two specimens of Helicolenus lengerichi (outgroup). These data were then combined with sequences from GenBank corresponding to 21 Sebastes species. Maximum likelihood and Bayesian phylogenetic approaches showed topological distinctiveness between South American and South African Sebastes populations, supporting the existence of two phylogenetic species: S. oculatus and S. capensis. However, Atlantic and Pacific populations of S. oculatus, did not form reciprocal monophyletic assemblages. Application of the Wiens & Penkrot's protocol to test species boundaries within this species did not support the existence of two different phylogenetic taxa. Gene flow between Atlantic and Pacific populations of S. oculatus could be explained by extensive larval dispersal, favored by both the Humboldt current and the West Wind Drift current along the South American coast.