Reviews in Aquaculture, 1–14 doi: 10.1111/raq.

12335

Advances in genetic improvement for salmon and trout

aquaculture: the Chilean situation and prospects

M. Ya
Jean P. Lhorente1, Marcelo Araneda1,2, Roberto Neira3 and Jose
n~ ez4,5
1 Benchmark Genetics Chile, Puerto Montt, Chile
2 Programa de Doctorado en Ciencias en Bioeconom
ıa Pesquera y Acu
ıcola, Centro Interdisciplinario de Ciencias Marinas del Instituto Polit
ecnico
Nacional, La Paz, M

exico
3 Facultad de Ciencias Agrono
micas, Universidad de Chile, Santiago, Chile
4 Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile
5 Nu
cleo Milenio INVASAL, Concepcio
n, Chile

Correspondence
Jos
e M. Y

an~ez, Facultad de Ciencias
Veterinarias y Pecuarias, Universidad de Chile,
Santiago 8820808, Chile.
Email: jmayanez@uchile.cl
Accepted 22 February 2019.
Abstract
Genetic improvement is key to the development of a more efficient aquaculture
industry. By 2010, there were 104 breeding programmes for aquaculture species
in the world, most of them for fish species. Usually, the breeding goals include
traits such as growth rate, disease resistance, maturation and carcass quality.
Resistance to specific pathogens has been one of the main objectives of research
and development in the genetic improvement programmes of salmonids in Chile
and worldwide. In Chile, trait selection has been conducted through the applica-
tion of selection indexes. New technologies like next generation sequencing and
genotyping have helped disentangle the genetic basis and enhance genetic evalua-
tion methods of economically important traits. This work aims to review the
advances in genetic improvement for salmon and trout aquaculture with empha-
sis on the Chilean experience. We focus on the implementation of breeding pro-
grammes in the country, definition of breeding objectives, results on genetic
parameters and response to selection and incorporation of genomics. Future chal-
lenges and opportunities regarding genotype-by-environment interactions, cli-
mate change and research and development, plus the demonstration of the
economic benefit of breeding programmes are also addressed.
Key words: breeding objectives, genetic improvement, genomic, salmon industry.

(i.e. genetic improvement programmes based on selective

Introduction
Salmon and trout farming in Chile started in 1986 with a
production of 2500 tons (Salgado 2005) and increased to
about 200 000 tons in 1996, 647 263 tons in 2006 and to
727 810 tons in 2016 (SERNAPESCA 1986-2016). Produc-
tion started with coho salmon (Oncorhynchus kisutch) and
rainbow trout (Oncorhynchus mykiss). Since the late 1990s,
industry growth has been based on Atlantic salmon (Salmo
salar), which is currently exceeding 70% of total salmon
and trout production in Chile (Fig. 1). Chile is currently
the second largest producer of salmon and trout in the
world, which positions the country as one of the top 10
exporters of fish products worldwide (FAO, 2016). This
paper reviews the advances in genetic improvement for sal-
mon and trout with emphasis on the Chilean experience; it
focuses on the implementation of breeding programmes
breeding) in the country, definition of breeding objectives,
results on genetic parameters, response to selection and
incorporation of genomics. We also provide an overview of
future challenges and opportunities, including genotype-
by-environment interactions (GxE), climate change,
demonstration of added value, research and development
priorities and market share direction.
First developments for the genetic improvement in
aquaculture
Aquaculture probably started in China about 4000–
5000 years ago (Gjedrem & Baranski 2009). Modern animal
breeding practices started at the beginning of the last cen-
tury, along with the theoretical development of quantitative
genetics led by the work of pioneers such as Sewall Wright

© 2019 Wiley Publishing Asia Pty Ltd 1

J. P. Lhorente et al.
Figure 1 Evolution of Chilean salmon industry production between 1986 and 2016 (SERNAPESCA 1986-2016).
in the 1920s and applied to animal production by Jay Lush,
with the first publication of his book ‘Animal Breeding
Plans’ in 1937. However, the first genetic improvement
programme based on families and sib data in aquaculture
species began 35–40 years after being used in terrestrial ani-
mals. This situation was mainly due to the fact that man-
agement and control of the complete reproductive cycle of
these species in captivity, an essential requirement to estab-
lish any formal breeding programme, were often very com-
plex and not well known (Gjedrem & Baranski 2009).
Among the most notable landmarks are the Atlantic salmon
and rainbow trout programmes developed in Norway by
AKVAFORSK in 1975 (Gjedrem 2000). Tilapia (Ore-
ochromis niloticus) breeding programmes started in 1989
with the project genetic improvement of farmed tilapia in
the Philippines, coordinated and implemented by ICLARM
(Ponzoni et al. 2011). The work on selective breeding in
coho salmon, which started in 1992 in Chile, developed by
the Institute for Fisheries Development (IFOP) and the
Universidad de Chile is also worthy of mention here (Neira
et al. 2004). Eastern Europe and Israel efforts on common
carp (Cyprinus carpio) selective breeding are also keystones
of modern fish breeding programmes (Hulata 1995). There
has been a significant proliferation of breeding programmes
in aquaculture species, and according to Rye et al. (2010)
and Neira (2010) there were up to 104 programmes in 20
species in 2010, including fish (82.6%), molluscs (8.2%)
2 © 2019 Wiley Publishing Asia Pty Ltd
and crustaceans (8.2%). Sixty-two of the breeding pro-
grammes are in developed countries (Rye et al. 2010), and
the rest have been established in developing countries
(Neira 2010). The five species with the highest number of
programmes were tilapia (n = 18), Atlantic salmon
(n = 13), rainbow trout (n = 13), carp (n = 8), shrimp
(n = 7) and oysters (n = 5).
The first salmon breeding programme in Chile
In Chile, the first coho salmon breeding programme was
established in 1992 by the IFOP and the Universidad de
Chile in Coyhaique, XI Region. The genetic basis of the
broodstock in Chile was Coho salmon eggs imported from
Oregon (USA) and the Kitimat River (British Columbia,
Canada) (Neira et al. 2014). The breeding programme con-
sisted of an independent tiered selection scheme for body
weight at harvest (~3 kg) and early spawning, measured in
days in females, in two independent populations represent-
ing even and odd spawning years. Initial studies were aimed
at the estimation of genetic parameters for reproductive
traits in females (Gall & Neira 2004), as well as growth and
carcass quality traits (Neira et al. 2004). Other studies
aimed to detect loci associated with relevant traits, includ-
ing meat colour and date of spawning (Araneda et al. 2005,
2009). Coho salmon farming in Chile was operating with a
2-year reproductive cycle, taking advantage of the water
Reviews in Aquaculture, 1–14

temperature (10°C) in lakes and other freshwater sources,
resulting in production of smolts in <1 year (Estay et al.
1997). After four generations of selection, there was a
response to selection of 9.9–10.5% gain per generation in
harvest weight (Neira et al. 2006a).
A phenotypic reduction of 13–14 days in the average
spawning date was obtained for the two selected year
classes, representing an average phenotypic response to
selection for spawning date of
3 days per generation
(Neira et al. 2006b). Using a mating scheme that avoided
mating full- and half-siblings, a cumulative inbreeding of
4.4% and 9.5% and an inbreeding rate of 1.1% and 2.4%
per generation were calculated in even and odd popula-
tions, respectively (Neira et al. 2006a). Environmental
dependence of inbreeding depression was also experimen-
tally identified on traits related to territorial dominance,
that is, the magnitude of inbreeding depression on an
experimental highly inbred progeny was modified by social
environment tested by using different culture densities
(Gallardo & Neira 2005). By using non-random mating
schemes, it is possible to control increases in inbreeding
and maintain genetic gain by applying optimization algo-
rithms in salmonids (Gallardo et al. 2004a; Yoshida et al.
2017b, 2018c). An independent study reported significant
inbreeding depression of the gonadosomatic index and
body length in females (5.3% and
1.56% for each 10%
increase in inbreeding, respectively) (Gallardo et al. 2004b).
Definition of breeding objective
The breeding objective should include traits that influence
income, expenses, or both, to increase profit. The main
trait in most breeding programmes is growth, followed by
disease resistance and carcass quality, including yield, fat
content, fat composition and flesh color (Neira et al. 2004;
Gjedrem 2005; Rye et al. 2010). When performing multi-
trait selection, the inclusion of the breeding objectives in a
single selection index is desired. A common problem in
programmes including multi-trait selection has been the
prioritization of the traits to be improved. According to
Ochsner et al. (2017), the prioritization must be based on
their economic relative importance. In this regard, there
are two approaches to deriving economic values:
1 The subjective approach uses the assignment of relative
values to illustrate consumer preferences when there is
no availability of economic or commercial data. The use
of this method is very common in aquaculture breeding
programmes (Bourdon 1998); however, it does not
involve the determination of the effect of each trait on
the profitability of the system.
2 The normative approach uses profit equations (PE) or
bio-economic models (Krupov
a et al. 2008). A PE is a
Reviews in Aquaculture, 1–14
© 2019 Wiley Publishing Asia Pty Ltd
Genetic improvements in salmon and trout
function that represents animal productivity (number of
individuals and biomass produced) and economic bene-
fit (Steine et al. 2008). Bio-economic models can be used
to better characterize the biological, technical and com-
mercial aspects of the farming process and analyse pro-
duction data over a period of time. This approach
applies dynamic simulation to establish production and
economic scenarios which determine the profitability of
the system (Ivkov
ıc et al. 2009).
For example, a PE for Atlantic salmon production in
the Chilean context was developed and it is shown in
Equation 1.
X5
p¼ d p N w Sð1
DÞ
No cf f
No csm
i¼1 i i o f

No cpr wf Sð1
DÞ
K ð1Þ
where p is the economic profit function in which income is
represented by number of end products after plant process-
ing (di); price vector of products (pi); initial number of fish
(No); target harvest weight (wf); survival at harvest (S); and
fillet yield after processing (D); and expenses are repre-
sented by total food consumption (f); fixed (K); food (cf),
smolt (csm) and processing plant (cpr) costs. Marginal eco-
nomic values (MEVs) are obtained by partially deriving the
PE from each trait, keeping the remaining variables con-
stant (Harris 1970). The MEVs for harvest weight (wf) are
obtained deriving p with respect wf as it is shown in Equa-
tion 2
@p
¼ MEVs ¼ No ½di pi Sð1
DÞ
cpr Sð1
DÞ ð2Þ
@wf
The advantage of PE is the simplicity in the formula-
tion and interpretation of results. However, the descrip-
tion of the aquaculture system by means of a single
equation could make it inaccurate because the longitudi-
nal nature of the farming process and stochastic variation
of different factors involved in the production output is
not considered. Figure 2 shows a scheme of the bio-eco-
nomic approach for the estimation of the MEVs. In
Chile, both bio-economic models and PE have been used
to estimate MEVs for salmon breeding programmes. The
implementation of bio-economic models is more suitable
when there is access to a considerable volume of produc-
tion and commercial data, which is rarely the case for
hatcheries supplying genetically improved salmon mate-
rial (i.e. eggs, fries and smolts). The goal is to have an
economic selection index to support the selection deci-
sions, defined as the sum of the products of the breeding
values (EVB) and MEVs for the traits considered within
the breeding objective.
3
J. P. Lhorente et al.

Biological State
sub-model instruments

Environment Economic
sub-model sub-model

Biotechnological Management
sub-model sub-model

Monte Carlo method

(2,000 random samples)

Figure 2 Steps of the bio-economic analysis approach to estimate marginal economic value (MEVxi) for salmon breeding programmes. (i) Productive,
environmental and economic data from a company or the industry are used to build biological, environmental, management, biotechnological and
economic sub-models; (ii) using system approach and including stochasticity, sub-models are linked into an integrated bio-economic model that
describes process of productive system and allows incorporate risk analysis considering the distribution of biological, biotechnological and economic
variables; (iii) productive unit size (company or industry), basic parameters of the productive system and restrictions of operation are defined to run a
simulation using bio-economic model; (iv) using Monte Carlo method with at least 2000 simulations, a probabilistic economic benefit function per fish
(pfish) which includes the traits into the breeding goal is estimated and (v) utilizing 2000 simulated data (p and breeding goals), a multiple regression
of p is calculated, then applying partial derivation MEV can be estimated for each trait considered into the breeding goal.

at harvest (Table 1). Genetic gains achieved are ~10% per

Genetic parameters and response to selection
Growth is the main breeding objective in salmonids (Rye
2012). The main selection trait is weight at harvest, which
in the Chilean production context is ~3 kg in coho salmon
and rainbow trout, and ~4.5–5.5 kg in Atlantic salmon.
Selection responses have been reported for breeding pro-
grammes around the world, in all three species for weight
generation.
To date, there is little information on the response to
selection for carcass quality traits. For instance, selection
response in fat content has been reported for rainbow trout
harvested pan-sized (260 g) (Quillet et al. 2005). Through
specific selection trials, Quillet et al. (2005) created high-
and low-fat lines and after two generations of selection saw

Table 1 Percentage of genetic gain (GG) for growth measured as harvest weight in salmon and trout breeding programmes in different countries

Species GG (%) Country References

Atlantic salmon 11–14 Norway Gjerde (1986), Gjedrem (2000)

7–15 Chile This study
Coho salmon 10 USA Hershberger et al. (1990)
9–10 Chile Neira et al. (2006a,b)
6–13 Chile This study; Dufflocq et al. (2017)
Rainbow trout 13 Norway Gjedrem (2000)
7–13 Chile This study

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4 © 2019 Wiley Publishing Asia Pty Ltd
 Genetic improvements in salmon and trout

a significant difference in muscle lipid content between the
fat and lean lines (29.6% and 25.6% dry matter content in
the fat and lean line, respectively). The same authors
showed that there are no differences in carcass and fillet
yield between fat and lean lines (Quillet et al. 2007). How-
ever, this should be further investigated on larger fish
(>1 kg) and other species.
Several studies have been carried out to estimate genetic
correlations between growth and carcass quality traits in
Atlantic salmon, rainbow trout and coho salmon (Table 2).
For example, a positive correlated response of flesh colour
to selection for growth is expected in Atlantic salmon (Gje-
drem 1997) and has been shown after eight generations of
selection in coho salmon (Dufflocq et al. 2017). In contrast,
other fillet quality traits, including per cent of fillet fat, pro-
tein, water and ash and flesh redness, are not expected to
be strongly modified by selection for increased growth rate
based on their low genetic correlation with body weight
(Kause et al. 2005).
Disease resistance
Breeding for disease resistance has been proposed as a
method to control outbreaks in aquaculture populations
~ez & Mart
ınez 2010; Ødeg
(Y
an ~ez et al.
ard et al. 2011; Y
an
2014b). Heritability values for resistance to the main dis-
eases affecting Chilean salmon and trout aquaculture have
been estimated (Table 3). Results from these studies are
positive and show that selection for resistance traits is a
potential method for disease control. The potential for
simultaneously improving multiple traits depends on the
genetic correlations between traits. A study in Atlantic sal-
mon determined a favourable genetic correlation
(
0.32  0.14) between resistance to Caligus rogercresseyi
and body weight, indicating that selection for increased
body weight will result in a lower parasite count (Y
an ~ez
et al. 2014a). In the same population however, there were
no significant genetic correlations between resistance to
Piscirickettsia salmonis and body weight or between resis-
tance to P. salmonis and C. rogercresseyi (Y
an ~ez et al.
2014a). In coho salmon, the presence of a moderately unfa-
vourable genetic correlation (
0.50  0.13) between time
to death due to P. salmonis infection and weight at harvest
was found (Y
an ~ez et al. 2016a). A similar study has deter-
mined the absence of significant genetic correlations for
resistance to C. rogercresseyi and P. salmonis with body
weight at harvest, and an unfavourable genetic correlation
(0.39  0.14) between the C. rogercresseyi count and time
to death caused by P. salmonis in rainbow trout. In the
same species, the absence of a significant genetic correlation
between resistance to infectious pancreatic necrosis virus
(IPNv) and body weight at harvest has been established
(Flores-Mara et al. 2017), These results indicate that there
is no clear pattern between the possible genetic associations

Table 2 Genetic correlations between growth measured as harvest weight (HW), carcass quality traits [slaughter weight (SW), length (L), condition
factor (CF), yield (Y), belly thickness (BT), gust fat (GF), gonad weight (GW)] and flesh quality traits [fillet fat content (FFC), pigment content (PC), value
of green-red component of CIELAB colour space measured with Minolta Chroma-metter (FCMCM) and flesh colour measured as SalmonFan score
(SFSc)]

SW L CF Y BT GW FFC PC FCMCM SFSc

HW 1.001 0.991 0.36(0.18)2 0.616 0.075 0.96(0.04)2 0.709 0.26 (0.39)8 0.363 0.4 (0.5)4 0.316
1.001 0.961 0.165 0.04 0.7610 0.2911 0.493 0.215
1.002 0.93 (0.03)2 0.587
SW 0.921 0.165 0.075 0.96(0.04)2 0.195
0.195
0.941 0.376 0.616 0.405 0.426
0.92 0.327
L 0.297
CF
0.095
0.015 0.045 0.646
0.516 0.646
Y 0.635
0.685 0.245
0.656 0.596
BT
0.385 0.245
0.736
GF
0.335
GW 0.002
FFC 0.273 0.083
PC 1.20 (0.36)3

Bibliographic references: (1) Gjerde and Gjedrem (1984); (2) Rye and Refstie (1995); (3) Bjerkeng et al. (1996); (4) Withler and Beacham (1994); (5)
Gjerde and Schaeffer (1989); (6) Rye and Gjerde (1996); (7) Iwamoto et al. (1990); (8) Elvingson (1992); (9) Gjedrem (1997); (10) Kause et al. (2007);
(11) Quinton et al. (2005).

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J. P. Lhorente et al.

Table 3 Heritabilities (h2) for the main traits included in breeding programmes for salmonid species

Species Trait h2 References

Salmo salar Harvest weight 0.15 Quinton et al. (2005)

Fillet yield 0.03–0.20 Gjerde and Gjedrem (1984); Rye and Gjerde (1996)
Flesh colour (Score) 0.14–0.20 Quinton et al. (2005); Vera et al. (2007)
Pigment content (ppm) 0.10–0.28 Quinton et al. (2005); Vera et al. (2007)
Fat content of flesh (%) 0.17–0.19 Quinton et al. (2005); Vera et al. (2007)
SRS resistance 0.10–0.34 Lhorente et al. (2012); Y
an
~ez et al. (2014a)
Caligus resistance 0.11–0.41 Y
an
~ez et al. (2013, 2014a)
Oncorhynchus mykiss Harvest weight 0.21–0.34 Gjerde and Schaeffer (1989); Rodr
ıguez et al. (2018)
Fillet yield 0.01–0.36 Gjerde and Gjedrem (1984); Gjerde and Schaeffer (1989)
Flesh colour (score) 0.27–0.33 Gjerde and Schaeffer (1989)
Fat content of flesh (%) 0.47 Gjerde and Schaeffer (1989)
IPNv resistance 0.39 Flores-Mara et al. (2017)
SRS resistance 0.44 Bassini et al. (2017)
Caligus resistance 0.09 Bassini et al. (2017)
Oncorhynchus kisutch Harvest weight 0.17–0.30 Neira et al. (2004)
Flesh colour (Score) 0.04–0.08 Dufflocq et al. (2017)
Fat content of flesh (%) 0.17–0.26 Neira et al. (2004)
SRS resistance 0.16 Y
an
~ez et al. (2016a)

for resistance to different diseases and other traits of pro-
ductive interest.
Structure of the Chilean salmon and trout egg
market
By 2010, 32 breeding programmes had been established for
salmonids worldwide (Rye et al. 2010). This situation has
resulted in that, for instance, ~97% of the worldwide pro-
duction of Atlantic salmon is currently based on genetically
improved stocks (Gjedrem et al. 2012; Robinson et al.
2017). Chile plays a key role in the international salmon
market and selective breeding is considered an important
tool in increasing the competitiveness of Chilean aquacul-
ture. The coho salmon breeding programme established by
IFOP and the Universidad de Chile in 1992 was created to
establish a centralized breeding programme to supply the
industry with genetically improved broodstock (FAO
1996). After this early initiative, the rapid growth of the
Chilean salmon industry has led to the establishment of
about 15 private breeding programmes for salmonid spe-
cies in the country, representing almost a half of the total
number of salmon and trout breeding programmes in the
world.
In Chile, commercial breeding programmes started being
established in the late 1990s. Atlantic salmon breeding popu-
lations were created mainly based on improved germsplasm
from Norwegian origin; however, North American and Scot-
tish material was also introduced for the same purposes
(Barr
ıa et al. 2018c; L

opez et al. 2018). Rainbow trout and
coho salmon Chilean breeding populations were established
based on improved germplasm introduced from multiple
origins and the west coast of North America (e.g. Oregon
and British Columbia), respectively (Neira et al. 2014; Barr
ıa
et al. 2018b). Due to the production crisis related to Infec-
tious salmon Anaemia outbreaks in 2007, currently, the
imports of new germplasm into Chile is banned, except for
countries which are declared free for the most important
pathogens affecting salmon aquaculture (e.g. Iceland). Cur-
rently, more than half of salmon and trout eggs produced in
Chile come from specialized egg suppliers belonging to com-
panies exclusively dedicated to the sale of genetically
improved eggs (e.g. AquaGen, Hendrix Genetics and Bench-
mark Holding). Another 30% of the improved eggs come
from integrated salmon companies with their own breeding
programmes (e.g. AquaChile, Camanchaca, Los Fiordos,
Marine Harvest). Currently, there is representation of local
and international breeding companies which are involved as
investors, suppliers of eggs and technical consultancy service
providers. Some national initiatives compete in quality and
technological capabilities with multinational suppliers; how-
ever, trends indicate that the salmon and trout egg market
will specialize and be concentrated to a few companies in the
near future. Consolidation will allow for higher production
volumes per company, making it possible to focus the
investment in research and development on creating breed-
ing and reproductive technologies at reasonable and com-
petitive costs.
Incorporation of genomics
The molecular basis of phenotypic variation for several eco-
nomically important traits in livestock species by means of
genome-wide association studies (GWAs) has been made

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6 © 2019 Wiley Publishing Asia Pty Ltd

possible by the development and application of novel geno-
mic techniques (Goddard & Hayes 2009; Blasco & Toro
2014). GWAs are conducted using a large number (i.e.
thousands) of single nucleotide polymorphisms (SNPs),
genotyped in a group of individuals with on which pheno-
typic data have been recorded in order to identify statistical
associations between them and a particular trait (Goddard
& Hayes 2009). If the proportion of variance explained by
significant SNPs is high, the associated markers can be used
to implement marker assisted selection (MAS) to speed up
the genetic progress (Hayes & Goddard 2010). If the pro-
portion of genetic variance explained by single markers is
low, information from a larger number of SNPs can be
used for a genomic selection (GS) approach. In a typical GS
scheme in salmon, individuals highly related to the selec-
tion candidates (i.e. full- and half- sibs) are genotyped and
phenotyped (known as a training population), while the
candidates are only genotyped (testing population). The
training population is utilized to estimate the effect of each
SNP, and genomic EBVs are predicted for the selection can-
didates using information from all genotyped SNPs
(Meuwissen et al. 2001).
Marker assisted selection and GS are complementary
approaches to traditional animal breeding techniques (i.e.
pedigree-based genetic evaluation) and their advantages are
primarily related with an increase in accuracy of selection
for traits which are difficult to measure on selection candi-
dates, including disease resistance and carcass quality traits,
and also potentially reducing time for selection where can-
didates can be selected at a young age based on the geno-
type (Sonesson & Meuwissen 2009; Villanueva et al. 2011;
Taylor 2014). Genomic resources, including high quality
reference genomes and dense molecular marker panels, in
the most important salmonid species farmed in Chile, have
been created in recent years, and they are expected to have
an important impact on unravelling the genetic basis of
complex traits and increasing the accuracy of selection
~ez et al. 2015). For instance, the International Collabo-
(Y
an
ration to Sequence the Atlantic Salmon Genome (Davidson
et al. 2010; Lien et al. 2016), has provided a reference gen-
ome sequence for Atlantic Salmon and a good basis for
sequencing other salmonids, including rainbow trout
(Berthelot et al. 2014; Gao et al. 2018), chinook (Chris-
tensen et al. 2018) and coho salmon (www.epic-4.org).
Genotyping by sequencing and whole genome re-sequen-
cing have been used to generate medium to high density
SNPs panels for Atlantic salmon (Houston et al. 2014;
~ez et al. 2016b), rainbow trout (Palti et al. 2015) and
Y
an
coho salmon (Ben Koop, pers. comm., 2018). Dense SNP
panels alongside powerful disease challenge experiments
have been used to perform GWAs for host resistance to two
of the most important diseases affecting Chilean salmon
and trout aquaculture: sea lice (C. rogercresseyi) (Correa
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Genetic improvements in salmon and trout
et al. 2017a,b) and Salmonid Rickettsial Septicaemia – SRS
(P. salmonis) (Correa et al. 2015; Barr
ıa et al. 2018a,c). Sea
lice resistance has been suggested to have polygenic nature,
given that it might be controlled by several markers of small
to moderate effect (Correa et al. 2017a,b), similarly to the
case of resistance against Leptoptherius salmonis, the north-
ern hemisphere sea louse species (Tsai et al. 2016).
Although genomic regions of moderate effect have been
detected for P. salmonis resistance in Atlantic (Correa et al.
2015) and coho salmon (Barr
ıa et al. 2018,a), they are most
likely not suitable for MAS, due to the relatively low per-
centage of the genetic variance explained by them. A major
quantitative trait locus (QTL) for resistance against IPN
has been identified (Houston et al. 2008) and successfully
implemented at a commercial level in European (Moen
et al. 2015) and Chilean stocks. Yoshida et al. (2017a) and
Neto et al. (2019) have also identified several genomic
regions and candidate genes associated with body weight in
Chilean Atlantic salmon and rainbow trout populations, as
it has been shown in previous studies (Gutierrez et al.
2015; Tsai et al. 2015; Gonzalez-Pena et al. 2016). Thus,
the opportunities for MAS are still likely to be limited com-
pared to GS in aquaculture because having few markers
explaining a large proportions of variation is rare in most
commercially important traits (i.e. they are mainly poly-
genic in nature), and the association is not always repeat-
able between different strains.
Genomic prediction methods are more accurate than tra-
ditional pedigree-based best unbiased linear predictor
(PBLUP) for EBV predictions for P. salmonis (Bangera
et al. 2017; Barr
ıa et al. 2018a,b,c; Yoshida et al. 2018a),
sea lice resistance (Ødeg ard et al. 2014; Tsai et al. 2016;
Correa et al. 2017a,b), bacterial cold water disease (Vallejo
et al. 2016, 2017) and IPN (Yoshida et al. 2019). Although
all of these studies demonstrate the feasibility of improving
the accuracy of EBV prediction, other factors have to be
considered for the practical implementation of GS. For
instance, the requirement of a large training population,
consisting of thousands of individuals with phenotypes and
genotypes, and the cost of genotyping a large number of
candidates to achieve an appropriate selection intensity are
most likely prohibitively expensive. However, the use of
genotyping strategies exploiting a combination of low- and
medium- density SNP panels and genotype imputation
have proven effective in increasing selection accuracy com-
pared to PBLUP while minimizing the costs of genotyping,
thus representing a cost-effective alternative for the imple-
mentation of GS in aquaculture species (Tsai et al. 2017;
Yoshida et al. 2018b). The increase in accuracy of selection
provided by GS for resistance to P. salmonis, sea lice and
other important diseases, will be of major commercial ben-
efit to the Chilean salmon farming industry. We believe
that the relative role of GS will express in adding value to
7
J. P. Lhorente et al.
existing traditional selection programmes which use phe-
notypic and pedigree information, and they are most likely
to be integrated by flexible approaches which exploit all the
information available in the whole breeding population
(i.e. pedigree, phenotypes and genotypes), such as single-
step genomic evaluations (Aguilar et al. 2011).
Future challenges and opportunities
Genotype-by-environment interaction
Aquaculture production is carried out under different envi-
ronmental conditions. The GxE interaction measures the
sensitivity of animals to changes in their environmental
condition, and how their genetic performance changes
under different environments (Falconer & Mackay 1996;
Gjedrem 2004). This change can generate re-ranking of
genotypes (i.e. individuals, families or strains) between dif-
ferent environments (Lynch & Walsh 1998). This means
that best genotypes in one environment (e.g. freshwater)
are not necessarily the best ones in other environments
(e.g. brackish water). Thus GxE can have an undesirable
impact on selective breeding because it may complicate the
prediction of EBVs and cause a loss of selection efficiency
(Gjedrem 2004). Therefore, GxE must always be considered
in genetic evaluation models (Mulder & Bijma 2005; Sae-
Lim et al. 2010). A comprehensive review on GxE interac-
tion in aquaculture species has indicated that differences in
rearing conditions led to strong re-ranking for survival in
Atlantic salmon and moderate to strong re-ranking for
growth in rainbow trout (Sae-Lim et al. 2015). A better
characterization of GxE interaction for growth and other
traits is still required in salmonids, in which specific envi-
ronmental factors that influence trait variation are tested
(e.g. water temperature, stocking density, salinity, photope-
riod, feeding regime and others).
Early on, it was assumed that salmon reared for breeding
programmes would have a grow-out phase in seawater con-
ditions. Therefore, growth of selection candidates was mea-
sured in similar conditions. New regulations implemented
post the sanitary crisis generated by the ISA virus between
2007 and 2009 in Chile, have required most broodstock to
switch to inland systems using input from freshwater
sources. Thus, some broodstock are reared under environ-
mental conditions that may be different from those at sea
sites; therefore, the presence of GxE is expected. If GxE
exists between growth measured at inland facilities and sea
sites, Chilean salmon breeding programmes should be
adapted to account for this interaction. This can be
achieved by having test stations at sea sites representing
one or more production environments, in which sibs of the
selection candidates are tested. Thus, pedigree- or geno-
mic-EBVs for growth under production conditions can be
included in the selection index.
8 © 2019 Wiley Publishing Asia Pty Ltd
Also, studies have shown low GxE interaction for disease
resistance traits measured under different rearing condi-
tions. For instance, when measuring resistance under con-
trolled challenge tests versus field outbreaks, low to
moderate re-ranking is expected for resistance to sea lice
(rG = 0.88) (Kolstad et al. 2005), furunculosis (rG = 0.95)
(Gjoen et al. 1997) and IPN (rG = 0.78–0.83) (Storset et al.
2007). Other specific environmental factors which can gen-
erate GxE for disease resistance traits, for example vaccina-
tion (Drangsholt et al. 2011) or coinfection of different
pathogens (Lhorente et al. 2014), have also been studied;
however, further studies are needed in order to evaluate a
broader range of environmental factors and pathogens.
This information will help to establish effective disease con-
trol plans using fish genetically improved for disease resis-
tance.
Climate change
It is expected that in the near future climate change will
affect aquaculture via various external factors including,
emergence of new diseases, frequency and severity of
weather events, seawater acidification, rising sea level and
changes in water temperatures (Shelton 2014 and see Soto
et al. this volume). The current stocks used for salmon and
trout culture may not be optimal in future conditions (Sae-
Lim et al. 2016). For instance, salmonids are poikilother-
mic organisms, which make them highly sensitive to
extreme changes in water temperature. A strong GxE in
growth of rainbow trout reared in different temperatures
has been reported (rG = 0.36), resulting in a substantial re-
ranking of breeding candidates (Sae-Lim et al. 2015). How-
ever, the way climate change will alter the production envi-
ronment is difficult to predict. It is unlikely that current
selection will enable anticipating all future challenges. It is
therefore important to maintain an effective population
size (Ne) to accommodate drastic changes in the environ-
ment. To ensure the long-term sustainability of a genetic
improvement programme, the minimum Ne is considered
to be 50 (Hall 2004), while the minimum Ne to retain the
evolutionary capacity of a population is considered to be
much higher at 500 (Franklin & Frankham 1998). A Ne
equal or greater than 500 is nearly impossible to achieve in
a single aquaculture breeding programme; however, it
could be achieved if several breeding programmes with the
same aim were genetically linked providing more resilience
of these populations to unexpected changes in future envi-
ronmental conditions (Y
an ~ez et al. 2014c).
Demonstration of added value
One important challenge for suppliers of eggs from geneti-
cally improved broodstock is to demonstrate that their
Reviews in Aquaculture, 1–14

customers will increase profits through the superior perfor-
mance of their fish. Well-designed performance tests pro-
vide a benchmark allowing short-term product validation
and a means to compare genetically improved products
from different suppliers. Ponzoni et al. (2013) reviewed
several benchmarking studies conducted on fish at the glo-
bal level. While statistically solid, they are all experimental
and studied on a small scale. Benchmarking initiatives
should be implemented on a commercial scale to allow
more realistic economical appraisal. Because the perfor-
mance of genetically improved fish can vary significantly
due to differences in environmental and management fac-
tors, it is difficult to infer performance based on data
obtained under commercial conditions. A good alternative
to evaluate genetically improved stocks at a production
scale is bio-economic approaches which can manage
stochastic variation and have been used for the economic
evaluation of technological developments (Araneda & Mir-
anda 2013).
Research and development
Rapid technological advances in genomics have allowed
improvements in selective breeding approaches during the
last decade. For instance, GS increased selection accuracy
compared to traditional pedigree-based selection in salmon
and trout. Although there is null published information
about objective economical appraisal of the implementa-
tion of GS in aquaculture breeding programmes, the devel-
opment and implementation of effective genotype
imputation strategies will promote the establishment of
cost-effective GS for traits that are difficult to measure in
selection candidates (Tsai et al. 2017; Yoshida et al.
2018b). Moreover, the identification of functional causative
variants, also called quantitative trait nucleotides (QTN),
will maximize genomic prediction accuracies (P
erez-Enciso
et al. 2015) within and across populations, decreasing the
need to obtain phenotypes for each generation and popula-
tion (i.e. year-classes) (Houston 2017). Combining differ-
ent sources of information, including GWAs,
transcriptomic [e.g. Robledo et al. (2018)] and re-sequen-
cing of whole genomes, will improve the identification of
QTN for polygenic traits, which is key for the international
initiative called Functional Annotation of All Salmonid
Genomes, which is aimed at generating a deeper under-
standing of the underlying biology and identification of
QTN for different economically important traits in salmo-
nids (Macqueen et al. 2017).
Gene-editing (GE) technology may revolutionize preci-
sion genetic engineering methods for a wide range of appli-
cations in all living organisms (Doudna & Charpentier
2014). For salmonids, the most likely application of GE is
related to increasing the frequency, and possibly fixation, of
Reviews in Aquaculture, 1–14
© 2019 Wiley Publishing Asia Pty Ltd
Genetic improvements in salmon and trout
favourable alleles segregating in major QTL affecting eco-
nomically important traits. Optimistically, improvements
in high-throughput GE methods may allow the modulation
of multiple QTN with moderate effect size (Jenko et al.
2015). In vitro GE systems (i.e. cell lines) may also be help-
ful for identifying and validating QTN underlying impor-
tant traits (Zhou et al. 2014). Studies on GE in salmonids
are still scarce. However, the successful inactivation of egfp
gene in CHSE cell lines (Dehler et al. 2016) and knockout
of the dnd gene which causes sterility in Atlantic salmon
(Wargelius et al. 2016), both generated by CRISPR-Cas9
system, reinforce the potential applications of this
approach. The practical implementation of GE methods for
precision breeding has still to be approved by regulatory
entities. A key issue is whether the resulting organism will
be classified as a genetically modified organism, as it has
recently been determined by The European Union (EU).
To date, GE is not specifically regulated in Chile; however,
main destination markets for Chilean salmonids are outside
The EU and, in general, involve countries which have been
more permissive with the production and commercializa-
tion of genetically engineered organisms. Therefore, the
enormous potential of GE to rapidly improve and reveal
the genetic factors and mechanisms underlying relevant
traits for salmon and trout make further exploration
worthwhile.
Rapid advances in research and development tend to
increase the complexity of newly discovered problems. It is
unlikely that breeding companies will maintain the ‘in
house’ multidisciplinary teams, infrastructure and
resources needed to keep them at the cutting-edge of
knowledge. Therefore, there should be a very strong inter-
action between industry and academia to generate solutions
in a timely manner and maintain competitiveness. Funding
agencies should aim to strengthen business-academia links
through appropriate methods.
Market share direction
Large economic investments in breeding programmes to
incorporate genomic tools and set up inland facilities,
have been required to ensure the high quality of eggs
from improved strains. These investments pushed the
industry to the consolidation of specialized egg suppliers
with high volumes of production, where the cost per
egg is highly diluted. Customers will notice the increased
value of the eggs and will learn what to expect from the
egg supplier in terms of product quality and perfor-
mance expectations. It is expected that selection indices
should be adapted and customized to each potential egg
buyer to reflect their specific requirements. For this rea-
son, strong technical assistance teams should be devel-
oped within each egg supplier company, as is the case
9
J. P. Lhorente et al.
of most important livestock genetic companies (Scott
Newman, pers. comm., 2014). This will ensure that the
value added by genetic improvement is reflected in pro-
duction. Thus, technical assistance will become a strong
commercial tool and will help differentiate suppliers of
improved eggs. The development of benchmarking pro-
grammes is essential to demonstrate added value.
Aspects such as feed conversion efficiency and high tem-
perature tolerance should be accounted for by genetic
improvement companies, with the aim of further
improving production efficiency and adaptation to cli-
mate change. We believe technical improvement in
genetic selection will drive market share in the near
future, with fewer companies competing for position in
the Chilean and global industry for improved salmon
and trout eggs.
Conclusions
Genetic improvement has been crucial for the development
of Chilean salmon and trout aquaculture industry. Eco-
nomically important traits including growth, disease resis-
tance, maturation and carcass quality are improved
through selective breeding using selection indexes. Geno-
mic information has helped to enhance genetic evaluation
methods and it is currently integrated into commercial
breeding programmes in Chile. Research and development
will be crucial to tackle future challenges including GxE
and climate change.
Acknowledgements
This work has been partially supported by N
ucleo Milenio
INVASAL from Iniciativa Cient
ıfica Milenio (Ministerio de
Econom
ıa, Fomento y Turismo, Gobierno de Chile) and
FONDECYT REGULAR No. 1171720.
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