Published April 13, 2017

BREEDING AND GENETICS SYMPOSIUM:

Climate change and selective breeding in aquaculture1
P.Sae-Lim,*2 A. Kause,† H. A. Mulder,‡ I. Olesen*
*Nofima Ås, Osloveien 1, NO-1431 Ås, Norway; †Biometrical Genetics,
Natural Resources Institute Finland, Jokioinen, FI-31600, Finland; ‡Animal Breeding and
Genomics Centre, Wageningen University & Research, 6700 AH, Wageningen, The Netherlands

ABSTRACT: Aquaculture is the fastest growing food above, 3 major adaptive strategies are identified. First,
production sector and it contributes significantly to general ‘robustness’ will become a key trait in aquacul-
global food security. Based on Food and Agriculture ture, whereby fish will be less vulnerable to current and
Organization (FAO) of the United Nations, aquaculture new diseases while at the same time thriving in a wider
production must increase significantly to meet the future range of temperatures. Second, aquaculture activities,
global demand for aquatic foods in 2050. According to such as input power, transport, and feed production
Intergovernmental Panel on Climate Change (IPCC) contribute to greenhouse gas emissions. Selection for
and FAO, climate change may result in global warm- feed efficiency as well as defining a breeding goal
ing, sea level rise, changes of ocean productivity, that minimizes greenhouse gas emissions will reduce
freshwater shortage, and more frequent extreme cli- impacts of aquaculture on climate change. Finally, the
mate events. Consequently, climate change may affect limited adoption of breeding programs in aquaculture is
aquaculture to various extents depending on climatic a major concern. This implies inefficient use of resourc-
zones, geographical areas, rearing systems, and species es for feed, water, and land. Consequently, the carbon
farmed. There are 2 major challenges for aquaculture footprint per kg fish produced is greater than when
caused by climate change. First, the current fish, adapt- fish from breeding programs would be more heavily
ed to the prevailing environmental conditions, may be used. Aquaculture should use genetically improved and
suboptimal under future conditions. Fish species are robust organisms not suffering from inbreeding depres-
often poikilothermic and, therefore, may be particularly sion. This will require using fish from well-managed
vulnerable to temperature changes. This will make low selective breeding programs with proper inbreeding
sensitivity to temperature more important for fish than control and breeding goals. Policymakers and breeding
for livestock and other terrestrial species. Second, cli- organizations should provide incentives to boost selec-
mate change may facilitate outbreaks of existing and tive breeding programs in aquaculture for more robust
new pathogens or parasites. To cope with the challenges fish tolerating climatic change.

Key words: adaptation, climate change, resilience, robustness, selective breeding

© 2017 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2017.95:1801–1812
doi:10.2527/jas2016.1066

INTRODUCTION

A major challenge to the growth of the global hu-

1Based on a presentation at the Breeding and Genetics Symposium man population is the food security. In 2015, Food and
titled “Resilience of Livestock to Changing Environments” at Agriculture Organization (FAO) of the United Nations
the 2015 Joint Annual Meeting held in Salt Lake City, Utah, reported that about 11% (or 814 million) of the world
July 19–23, 2016. This work is a part of SmartSea project “Gulf population were undernourished (FAO et al., 2015).
of Bothnia as Resource for Sustainable Growth” funded by the More importantly, the world population will increase
Strategic Research Council of Academy of Finland. to 9.7 billion by 2050 (United Nations, 2015). To meet
2Corresponding author: [email protected]
the rising demand, the global agricultural production
Received September 26, 2016.
must increase by 60% globally (Nwanze et al., 2012).
Accepted December 17, 2016.
1801
1802 Sae-Lim et al.

To increase the global food production, an expansion

in sustainable agriculture is required. Nevertheless, the
land-based agricultural production is limited in resources
while aquaculture offers considerable potential in food
production (Kutty, 2009) because 72% of earth surface
is water. So far, inland freshwater, accounted for 1% of
the earth surface, has been the main area used for aqua-
culture (FAO, 2016). Aquaculture is the fastest growing
sector of food production, contributing substantially to
global human food supply (Gjedrem et al., 2012). It has
been concluded that ocean’s fisheries are no longer sus-
tainable (Pauly et al., 2002; Marra, 2005; Brander, 2007), Figure 1. World aqauctic animal productions from fishery and aqau-
and aquaculture therefore plays an increasing and major culture during 2005 and 2014. This bar is plotted using the statistical data
from Food and Agriculture Organization of the United Nations (FAO,
role in the global aquatic animal production (Fig. 1). 2016). From this figure, the growth rate of aquaculture production is 3.26
It is undeniable that aquaculture production depends million t per year (slope of linear regression), indicating that aquaculture
on rearing conditions and uncertainties due to climate production is reaching fishery production by 2020.
change. Climate change may result in global warming,
saline water intrusion, water stress, and ocean acidi-
fication, all of which may affect aquaculture (De Silva vironments, and climatic zones. A change of climatic
and Soto, 2009). Until now, the potential of selective zone can result in positive or negative impacts or both
breeding to cope with impacts due to climate change on (De Silva and Soto, 2009). Hence, climate change may
aquaculture and the bioeconomy has not been discussed. introduce potential opportunities, as well as, several
Therefore, we present here the possible solutions that challenges to aquaculture.
selective breeding can deliver to aquaculture. We first
briefly summarize the impact of climate change on aqua- Opportunities
culture before we discuss adaptive measures by aquacul-
ture breeding, involving the breeding goal and breeding Rise of water temperature may prolong the growth
strategies, as well as governance and political economy. period for animals, especially in temperate regions.
Consequently, aquaculture production may increase for
MAJOR IMPACTS aquatic species farmed in temperate zones. Furthermore,
change in water temperature is expected to change wild
Impact of climate change on aquaculture can vary fish stock communities. For example pelagic fish spe-
with respect to both type (e.g., water temperature, saline cies are expected to migrate poleward (Barange and
water intrusion, ocean acidification) and extent of cli- Perry, 2009). Therefore, new fish species could poten-
mate change, depending on climatic zones (temperate, tially be farmed in specific environments where the
arid, tropical, or Mediterranean), geographical areas new fish species previously were not farmed because
(inland, sea, or coastal), types of aquaculture produc- of environmental conditions (Bergh et al., 2007). With
tion systems, and aquatic species that are farmed. In respect to disease outbreaks, diseases associated with
the Northern Hemisphere, the increased temperature cold water [e.g., winter ulcer in Atlantic salmon (Salmo
may result in mild climate and positive effects on an- salar L.) caused by Moritella viscosa] could be less fre-
imal growth but may also introduce new diseases. In quent due to warmer water temperature.
the Southern Hemisphere, increased temperature may
result in heat stress, flood, drought, and more extreme Challenges
climates (De Silva and Soto, 2009). Moreover, the
ocean productivity is projected to decline due to climate There are several major challenges associated with
change and raw materials for fish meal and fish oil may climate change to aquaculture. The effects of climate
be in shortage (Schmittner, 2005; De Silva and Soto, change mainly affect production and welfare traits,
2009). In this circumstance, climate change indirectly such as growth and survival of farmed organisms in
puts more pressure on the improvement of feed effi- the presence of environmental stresses and (new) dis-
ciency-related traits, especially in carnivorous species. ease outbreaks.
As fish fecundity is high, it allows for distribut- Reduction in Growth and Survival. Most fish
ing genetically improved fish from a single breeding species are poikilothermic creatures as fish have a
program to international or even global producers that body temperature that varies with the temperature
may vary greatly with respect to market, farming en- of their surroundings. In nature, fish can move ver-
 Breeding for resilience to climate change 1803

tically in the water column to control body tempera-

ture. Nonetheless, this natural process of controlling
body temperature may be limited for fish farmed in
captive environments and small water bodies. This
implies that effects of climate change on finfish and
shellfish can be even greater than on terrestrial live-
stock. Production traits in fish may be highly sensitive
to environmental changes. When the mean ambient
water temperature changes toward the upper or lower
biological limit of a fish species, fish growth can de-
crease dramatically (Mallet et al., 1999; Neuheimer et
al., 2011; Fig. 2). There are reports showing negative
effects of increased water temperature on growth and
overall survival, especially during summer. For ex-
Figure 2. Graphical presentation of biological growth curve using
ample, in rainbow trout (Oncorhynchus mykiss), a wa- Mallet growth function (Mallet et al., 1999) on a simulated data. The Tmin
ter temperature increase of 2°C lessened appetite and (4°C) and Tmax (25°C) are minimum and maximum water temperature
growth in late summer (Dockray et al., 1996; Linton points that animals are at their biological limit to grow. Topt (19°C) is an
optimal water temperature point where growth rate is at maximum level.
et al., 1997; Morgan et al., 2001). Increased water The blue and red arrows represent water temperature changes due to cli-
temperature led to 25% summer mortality of farmed mate change toward lower and upper biological limits of animal, respec-
abalone (Haliotis spp.) in Australia, which resulted tively, which reduce growth rate substantially.
in economic loss at AUS$1.75 million (N. Robinson,
Nofima AS, Norway, personal communication).
Likewise, increased water temperature causes summer climate change, because genotype-by-environment in-
mortality of Pacific oyster (Crassostrea gigas; Cheney teraction (G × E) may occur. The G × E may lead to
et al., 1998; Samain et al., 2007; Malham et al., 2009). less-than-expected genetic gains in production envi-
Summer mortalities in Pacific oyster generally occur ronments due to that the genetic correlation between
at a rate of approxiamtely 10 to 15%, but high summer optimal environments and productions environments
mortality rates (80%) have been reported (Berthelin is less than one (Falconer, 1952; Mulder and Bijma,
et al., 2000), for example, in Tomales Bay, California 2005; Sae-Lim et al., 2013, 2015b).
(Burge et al., 2007). In oysters, a rise of sea-surface temperature can
More Frequent Disease Outbreaks. Changing en- also change spatial distribution of disease outbreaks,
vironmental conditions due to climate variability may facilitating new diseases to emerge (Harvell et al.,
increase prevalence and virulence of existing diseases. 1999, 2002). In the U.S., warming winters on the east
Warmer water temperature can introduce heat stress to coast (Polovina et al., 1994) may expand oyster dis-
animals, which can depress their immune system lead- eases (Haplosporidium nelsoni; Ford, 1996; Cook et
ing to greater susceptibility to diseases. In addition, al., 1998). An increased water temperature trend in the
pathogens become more virulent because many patho- ocean could expand Perkinsus marinus, the causative
gens grow faster at higher temperature (Marcogliese, agent of Dermo disease, northward (Ford, 1996).
2001). In wild salmon, several parasites and bacterial Difficulty in Exoskeleton Development. Ocean
diseases become more virulent in higher water tem- acidification may potentially impact mollusk culture
perature (McCullough, 1999; Crozier et al., 2008). because it is difficult for shellfish, such as clams, oys-
In Mozambique tilapia (Oreochromis mossambicus), ters, and mussels, to build shells (or exoskeletons, in the
mortality to Streptococcus iniae increased significant- case of crustaceans). An obvious example is the experi-
ly to 50% and 55% when water temperature increased ment with sea urchin (Tripneustes gratilla) by Sheppard
to 35°C and decreased to 19°C, respectively (Ndong Brennand et al. (2010). Decreasing pH from 8.15 (con-
et al., 2007). In contrast, mortality was only 13% trol level) to 7.6 (acidified condition), as a simulated
when water was at the optimal temperature of 27°C ocean acidification, showed significant reduction in sea
(Ndong et al., 2007). This indicates that resistance to urchin larval development due to decreased skeletal
Streptococcus iniae at optimal water temperature may length of larva body (Sheppard Brennand et al., 2010).
be genetically considered as a different trait from re- In 2014, mollusk culture production was 16.1 million t,
sistance to Streptococcus iniae under suboptimal water which accounts for 21% of global aquaculture produc-
temperature. Breeding for survival to diseases at opti- tion (FAO, 2016). Thus, any negative impacts on shell
mal temperature may not necessarily improve survival development could affect global aquaculture produc-
to diseases in production environments influenced by
1804 Sae-Lim et al.

tion substantially. This has, however, received little at-

tention (De Silva and Soto, 2009).

ADAPTIVE MEASURES

Climate changes affect the ecosystem services that

both aquaculture and the society in general are depen-
dent on. Because the monetary impact of climate change
and reduced ecosystem services are not reflected in the
current aquaculture product prices and costs in the mar-
kets, it has been argued that “they have been ignored or Figure 3. Graphic representation of 3 major adaptive strategies from
undervalued, leading to the error of designing breeding selective breeding to cope with effects of climate change on aquaculture.
schemes whose social or ecological costs may outweigh The three major adaptive strategies also aim to minimize the impact of
their benefits” (Olesen et al., 2000). Animal breeding aquaculture on climate change, for example, to reduce greenhouse gas
emissions through reduction in environmental loads, and moving aquacul-
for sustainable production systems requires that envi- ture toward greater efficiency and greater sustainability.
ronmental and social concerns are taken into account,
and, hence, values other than economic and short-term
benefit must be considered (Olesen et al., 2000). change may introduce more frequent unpredictable
Climate change may imply needs for changes in the fluctuation or variation in environmental factors or ex-
breeding goal and changes in the related governance treme weather that can vary across years or generations.
and political economy involved. Also, as animal breed- When defining robustness for fish breeding, the na-
ing is a long-term process and the predictions of climate ture of production environments in aquaculture has to be
change are still very uncertain while representing great taken into account in the context of climate change. In
hazards, risks and governance also need to be consid- aquaculture, aquatic animals are generally farmed under
ered. Aquaculture will need to be more ‘resilient’ un- natural environmental conditions during grow-out peri-
der fluctuating global climate conditions. The aim will ods in combination with diverse production systems in
probably not be to make one-size-fits-all animals but different geographical locations. Hence, several environ-
rather select and breed for animals that can survive and mental factors such as temperature, dissolved oxygen,
thrive better under uncertainties of climate. and pH are impossible to control in most aquaculture pro-
To cope with the effects of climate change on duction systems. Consequently, aquatic animals may be
aquaculture, three key adaptive measures are present- exposed to a great variation in environmental factors and,
ed and discussed here: breeding for robustness, reduc- hence, animals need to be robust. With climate change,
tion of environmental impacts, and adoption of selec- such pressure on animals to be robust may increase even
tive breeding (Fig. 3). more due to the potential increase in variation in environ-
mental factors. Current and new diseases may be favored
Breeding for Robustness by environmental changes as mentioned above and pose
more risk to fish health and welfare.
Definition of Robust Animals in Aquaculture. In Hence, for robust fish, we need to put emphasis not
biology, robustness is termed as “a property that allows only on a greater virulence of current diseases, but also
a system to maintain its functions despite external and potentially new diseases, as well as on the homeostasis
internal perturbations” (Kitano, 2004). Robustness of high production potential in the diverse grow-out en-
does not mean to stay unchanged so that the biological vironments and managements. Robustness has been dis-
functions are unaffected but robustness is the mainte- cussed and defined for pigs (Knap, 2005), poultry (Star et
nance of specific biological functions against pertur- al., 2008), and dairy cattle (Ten Napel et al., 2009). Three
bations (Kitano, 2004). Next to robustness, adaptation key characteristics in their definitions of robustness are
of animals is important and refers to the ability of a high production potential, adaptation to a wide range of
species to adapt to an environment. production environments or homeostasis, and a short pe-
In animal breeding, robust animals are able to grow riod to recover. Robust fish could be defined as an ani-
and keep functioning in the presence of environmental mal that is less vulnerable to current and new diseases
variation while adaptive animals are able to change in and parasites, while at the same time thriving in a wider
response to gradual changes in mean of environmen- range of production or farming environments.
tal cues, such as temperature. Indeed, both robustness Breeding Goal for Robustness. To breed for ro-
and adaptation are important characteristics for animal bustness, the breeding goal may change to breed for
breeding, but robustness is more relevant as climate more robust animals; new breeding goal traits may be
 Breeding for resilience to climate change 1805

added, and the index weights per trait may change as

well. For instance, the breeding goal may be extended
to traits such as environmental sensitivity, disease re-
sistance and tolerance. Furthermore, climate change
may lead to a greater uncertainty of the importance of
traits in the breeding goal, for example, variability in
economic values of traits (Rose et al., 2015).
Environmental Sensitivity. Genotypes that main-
tain homeostasis in a wide range of aquaculture pro-
duction environments are not sensitive or plastic to en-
vironmental change. From an animal breeding point of
view, environmental sensitivity for production traits,
such as growth, can be quantified as the slope of a re- Figure 4. Reproduced reaction norm of growth in rainbow trout
action norm while the intercept is the performance of (Oncorhynchus mykiss) across different levels of water temperatures (Sae-
an animal in an average environment (Stearns, 1989; Lim, 2013). A total number of ten sires were chosen randomly. The Y-axis
is the sire estimated breeding value for body weight and the X-axis is the
de Jong, 1995, 1990). Flat reaction norms indicate less water temperatures.
sensitivity to environmental changes, whereas posi-
tive or negative slope refers to genotypes that respond
to environmental changes positively or negatively. Cold tolerance is of importance and there is an indi-
Genotypes may have different levels of environmental cation of genetic variation in this trait, for example in tila-
sensitivity. A presence of G × E or non-parallel reac- pia (Cnaani et al., 2000). Heritability for survival to cold
tion norms is an indicator that there is genetic variation stress was estimated to be 0.20 in red drum (Sciaenops
in environmental sensitivity and that selective breed- ocellatus; Saillant et al., 2008). In contrast, heritability
ing for environmental sensitivity is possible. The ge- for survival of Chinese fleshy prawn (Fenneropenaeus
netic correlation between intercept and slope impacts chinensis) under cold water temperature challenge test
the magnitude of correlated response in environmental was low (0.02 to 0.06; Li et al., 2016).
sensitivity when selecting for growth in the average To gain more understanding, we calculated rg be-
environment in which the intercept is placed. tween intercept and slope of reaction norm using the
Due to climate change, one of the most common results from the reaction norm model on harvest body
water variables that changes and influences farmed weight of rainbow trout (Fig. 4) from a previous study
aquatic animals is water temperature. Thus, heat and (Sae-Lim, 2013; Sae-Lim et al., 2014). The rg between
cold tolerances are relevant traits for robustness. There growth and thermal sensitivity is negative and close to
is some evidence in aquaculture indicating that varia- minus unity (-0.95), indicating a substantial tradeoff
tion in thermal tolerance is partly explained by genetic between response to selection for growth and ther-
effects. In Atlantic salmon (Salmo salar L.), high phe- mal sensitivity. This rg, regardless of the sign, is of
notypic variation of relative ventricle mass at a critical greater magnitude than rg between production traits
maximum temperature between families and notice- and thermal or environmental sensitivity reported in
able similarity among siblings were observed, indicat- previous studies for growth (-0.33 to -0.42) in rainbow
ing that there is genetic variation in thermal and hy- trout (Sae-Lim et al., 2015a), test-day-milk (-0.36 to
poxic tolerance (Anttila et al., 2013). In rainbow trout, -0.47) in Holstein dairy cows (Ravagnolo and Misztal,
the first evidence of family by temperature interaction 2000; Aguilar et al., 2009), fat yield (-0.30 to -0.39)
(7°C and 15°C) was quantified and reported (genet- in Holstein dairy cows (Aguilar et al., 2009), protein
ic correlations or rg = 0.18 to 0.54) by McKay et al. yield (-0.36 to -0.50) in Holstein dairy cows (Aguilar
(1984). Sae-Lim et al. (2014) reported absent to strong et al., 2009), and carcass weight (-0.50) in finishing
genotype re-ranking at four different levels of water pigs (Zumbach et al., 2008). Most reported rg between
temperature for growth in rainbow trout (rg = 0.61 to production traits and heat tolerance indicate that the
0.99) using a reaction norm model. In European sea- genotypes with high production capacity are more sen-
bass (Dicentrarchus labrax), strong genotype re-rank- sitive to heat stress. This is in line with the conclusion
ing (rg = 0.49) of growth in 2 different levels of water from previous studies, for example by Kolmodin et
temperature (13°C and 19°C) was reported (Saillant al. (2002), that selection for a genotype’s high perfor-
et al., 2006). The previous studies indicated the pres- mance will increase environmental sensitivity in that
ence of genetic variance in slopes of the reaction norm genotype. However, the opposite trend was reported
on temperature, showing the possibility for selective for farrowing rate (-0.36 to 0.16) in pigs from different
breeding to increase heat tolerance. dam lines (Bloemhof et al., 2012). The rg were around
1806 Sae-Lim et al.

zero, indicating that simultaneous selection for greater Nile tilapia (Oreochromis niloticus), and rainbow trout.
farrowing rate and less sensitivity to heat stress is pos- The magnitude of G × E for survival seems even greater
sible (Bloemhof et al., 2012). Similar evidence was than for growth (Sae‐Lim et al., 2015b).
observed in tilapia for which the correlation between Increased water temperature together with disease
fish size and cold tolerance was reported to be zero outbreak will lead to more challenging production en-
(Cnaani et al., 2000). Likewise, rg between survival to vironments for fish to grow because not only growth
cold water temperature challenge test and growth was performance but also survival to increasing pathogen
zero in Chinese fleshy prawn (Li et al., 2016). burden may decrease. To cope with increased water tem-
In fish breeding, studying the genetics of heat and perature due to climate change, we need to improve our
cold tolerance in aquaculture lags far behind livestock understanding by introducing an interaction between wa-
species. In addition, tolerance to other environmental ter temperature and pathogen burden into a disease-chal-
factors, such as acidification, has been explored with- lenge test for which the genetics of tolerance for growth
out using a reaction norm perspective. The review by and survival can be studied simultaneously. To date, such
Gjedrem and Rosseland (2012) reveals the presence a study has not yet been conducted in aquaculture.
of genetic variation for tolerance to acidic waters in Uncertainty in Climate and Breeding Goal.
different species of salmonids. No study, however, has Climate change is very difficult to predict, due to com-
quantified genetic parameters for acidic tolerance in plex interactions between changes in the mean and vari-
mollusks or crustaceans. More empirical studies are ability, resulting in uncertainty in climate predictions
needed to quantify genetic variation in tolerance of (Folland et al., 2001). In 2011, the Intergovernmental
production and reproduction traits to environmental Panel on Climate Change (IPCC) demonstrated 3
changes in aquaculture to increase our understand- scenarios of change in mean and variability of tem-
ing of the genetics of tolerance and to design optimal perature (Folland et al., 2001; Fig. 5). The increase
breeding schemes to breed for robust animals. in mean temperature leads to new records of high
Disease Resistance and Tolerance. Disease re- temperature (Fig. 5A) while the increase in variabil-
sistance and tolerance are 2 different mechanisms of ity without change in mean temperature implies the
host’s response to infectious diseases (Doeschl-Wilson greater probability of hot and cold extremes (Fig. 5B).
et al., 2012; Kause and Ødegård, 2012). Disease re- Finally, increase in both the mean and the variability
sistance refers to an ability of host organisms to limit affects the probability of hot and cold extremes with
a number of pathogens (or pathogen burden) in the more frequent heat waves, more extreme hot weather
host organism. In other words, a more resistant fish but fewer cold events (Fig. 5C). Other combinations
will have lower pathogen burden than a less resistant of changes in both mean and variability would lead to
fish. Tolerance refers to the ability of the host organ- different changes in temperature (Folland et al., 2001).
ism to maintain their performance during periods of Uncertainties in climate may introduce risk to aqua-
increased levels of pathogen burden. Tolerance is the culture because current economic values or relative
slope of reaction norm on its pathogen burden for weighing factors in a breeding goal may not necessar-
which a genotype with zero or positive slope is a toler- ily reflect the most profitable animals in a given future
ant genotype (Kause and Ødegård, 2012). production system influenced by the effects of climate
In aquaculture, many studies focus on genetics of change. In this regard, genetic responses of breeding goal
survival in a disease challenge test for which it is im- traits may vary due to uncertainty of climate. Breeding
possible to disentangle the genetic effects for resistance goals may have to adapt to uncertainties of climate, both
and tolerance. Survival may be due to resistance as the in terms of breeding goal traits and their economic values.
pathogen burden is assumed to be at constant level for Rose et al. (2015) demonstrated that different climatic
all animals during a challenge test period. In contrast, zones may experience uncertainty in pasture growth, and
increased water temperature due to climate change may consequently, economic values change to maintain prof-
increase associated-warm-climate pathogen burden and its in sheep farming. Rose et al. (2015) recommended
consequently disease tolerance will be increasingly im- customizing a breeding goal to ensure the most profitable
portant in production environments. Thus, selection for sheep for uncertain production environments.
survival to a specific disease challenge test based on To address risks due to climate uncertainty, it is im-
the controlled environment may result in less surviv- portant for a breeding company to take their customer’s
al to the disease in the production environment. Sae- production environments and effects of climate change
Lim et al. (2015b) reviewed the magnitude of G × E in into account when redefining their breeding goals. It is
aquaculture and found strong genotype re-ranking for arguable whether a single breeding goal can cover the
survival in different locations (rg = 0.17 to 0.98) and wide range of markets and production environments un-
rearing systems (rg = 0.32 to 0.90) in Atlantic salmon, der climate change. Specific breeding goals can be de-
 Breeding for resilience to climate change 1807

Reduction in feed production and reduced amount

of feed needed for producing each kg of fish can re-
duce global warming potential (d’Orbcastel et al., 2009;
Buchspies et al., 2011). In addition, fish meal and fish
oil are the major ingredients for protein and energy
resources in fish feed for farmed fish and shrimp spe-
cies. Raw materials for fish meal and fish oil produc-
tion are mainly from the wild fish stocks. An increased
use of fish meal for feed production may contribute to
overfishing and influence natural ecosystems. Selective
breeding can offer 3 possibilities; selection for feed effi-
ciency, selection for animals that can adapted to alterna-
tive ingredients for protein resources, and implementa-
tion of life cycle analysis when defining breeding goals.
Selection for Feed Efficiency. Selective breeding
for increased production, such as growth, is expected
to enhance efficiency of feed utilization, through cor-
related changes in feed efficiency; therefore, selec-
tion for increased growth rate can be used to improve
feed efficiency. However, many studies have quanti-
fied genetic variation of feed efficiency and indicated
the possibility to perform direct selection. In rainbow
trout, coefficients of additive genetic variation for
feed conversion efficiencies were low to moderate (4
to 14%), indicating that improving feed conversion ef-
ficiencies through selective breeding can be successful
(Henryon et al., 2002). Similarly, the mean heritability
for daily feed intake was over 0.10, indicating that ge-
netic changes can be expected from selective breeding
Figure 5. Graphical presentation of changes in mean and variabil- (Kause et al., 2006). Thodesen et al. (1999) compared
ity of temperature. This figure is reprinted from Intergovernmental Panel growth and feed conversion efficiency of Norwegian
on Climate Change (Reprinted with permission of Intergovernmental
wild and farmed Atlantic salmon from five generations
Panel on Climate Change-Climate Change 2001: The Scientific Basis.
Contribution of Working Group I to the Third Assessment Report of the of selective breeding since in 1979. They reported
Intergovernmental Panel on Climate Change, Technical Summary, Fig. that feed conversion efficiency increased by 23% in
2.32. Cambridge University Press, Cambridge, United Kingdom). farmed fish after five generations compared with wild
fish. This improvement is further extrapolated to 30%
fined for animals that can best adapt to a group of simi- after ten generations in 2014 (T. Gjedrem, Nofima AS,
lar and specific production environments while a broad Norway, personal communication). Gjedrem (person-
breeding goal can be defined to cover a wide range of al communication) indicated that selective breeding
farming environments. A decision on having specific or resulted in 0.5 million t reduction in feed production
broad breeding goals or both may depend on the scope per yr compared with feed requirement in 1979. This
of the customer’s production environments and the mag- clearly shows the benefit of selective breeding on feed
nitude of effects due to climate change on aquaculture. efficiency, reducing the impact of aquaculture on cli-
mate. Further studies on genetic effects of feed effi-
Reduction of Environmental Loads ciency in other aquatic species are needed.
Adaptation to Novel Ingredients. Feed manufac-
One of the key aspects of sustainable aquaculture turers have gradually replaced fishmeal with alterna-
is to minimize environmental impact (Olesen et al., tive protein sources. To date, only 30% of Norwegian
2011). Although aquaculture has no direct impact on salmon feed ingredients are from marine origin, where-
climate change because aquatic species do not emit as the remaining 70% are from plant origin (Ytrestøyl
greenhouse gasses (GHG) as do ruminants, aquacul- et al., 2015). Replacing dietary ingredients with fu-
ture activities, such as logistics, input power, and feed ture materials, such as novel plant-based ingredients,
production indirectly affect climate change. may introduce G × E of growth and feed efficiency
in breeding stocks. For growth, genotype re-ranking
1808 Sae-Lim et al.

was strong to absent (rg = 0.55 to 1.00) in rainbow Aquaculture based on wild stocks that are not
trout (Le Boucher et al., 2011a) and European sea- adapted to the farm environment, or farmed animals
bass (Le Boucher et al., 2011b), whereas genotype re- from breeding programs without proper selection
ranking was absent in European whitefish (Coregonus and(or) control of inbreeding rate, will lead to poor
lavaretus; Quinton et al., 2007). For feed efficiency, performance and survival compared with genetically
genotype re-ranking varied from strong to absent (rg improved or well-managed stocks. This implies low
= 0.63 to 0.99) in rainbow trout (Kause et al., 2006), aquaculture production and inefficient use of resources
whereas weak or absent re-ranking was observed in for feed and land. Consequently, the carbon footprint of
European whitefish (Quinton et al., 2007; Kause et al., aquaculture is greater and the negative effect on climate
2008). Strong re-ranking indicates that genotypes may is larger than when only selected stocks would be used.
be sensitive to dietary replacements, and growth and Aquaculture should use genetically improved and
feed efficiency on different diets are genetically differ- robust species not suffering from inbreeding depression.
ent traits. Selection for genotypes that perform well This will require using fish materials from well-managed
on novel dietary compositions will improve adapta- selective breeding programs with proper breeding goals
tion and reduce the use of marine ingredients. and a controlled rate of inbreeding. For full implementa-
Life Cycle Analysis. Life cycle analysis (LCA) is tion of genomics to boost aquaculture breeding further,
a method to quantify the use of resources and emission there first must be a proper selection program in place.
of pollutants of the entire production chain for a prod- Animal breeding programs have been shown to pro-
uct. Applications of LCA to define breeding goals that vide long-term impacts and benefits for food production,
maximize production, while minimizing environmen- which also represents a valuable public good. For plan-
tal impacts can be one solution (Besson et al., 2016). ning of breeding programs and choice of breeding strat-
Recently, Besson et al. (2016) combined LCA with a egies, private breeding companies usually discount the
bio-economic model to derive economic and environ- value of future income from breeding to its value at the
mental values when defining a breeding goal for African time of investment in breeding. For this, discount rates of
catfish (Clarias gariepinus) and found that selection for approximately 5% have been applied (Smith, 1978). The
growth rate and feed conversion ratio in catfish reduced uncertainty of the future production environment and
GHG emission and other environmental loads. With the framework conditions due to climate changes introduce
methodology of Besson et al. (2016), it is possible to an additional uncertainty and risk of private investments
evaluate different breeding strategies that maximize to- in breeding. However, from the perspective of the society,
tal genetic gain and minimize environmental loads. the public goods in terms of nutrient value of increased
fish production and importance of strengthening food
Adoption of Selective Breeding security will be the same in, for instance, 30 yr in the
future as it is today. To stimulate the adoption of, and pri-
Setting up a breeding program is the first step prior vate investment in, sustainable aquaculture breeding to
to implementing selection for robustness, reduction of strengthen long-term food security, the need for public
environmental impact, and adapting aquaculture to support of breeding programs should be considered by
climate change. Different magnitudes of genetic gain the governance, as also noted by Olesen et al. (2015). In
for growth and survival traits have been reported in this connection, the choice and development of appropri-
several aquatic species. For growth traits, genetic gain ate business models for breeding is also important to se-
(increase per generation) averaged 17.8% in Atlantic cure profitable breeding investments and supporting sus-
salmon, 12.0% in tilapia, 9.0% in rainbow trout, and tainable aquaculture production (Olesen et al., 2015). For
14.5% in channel catfish (Ictalurus punctatus). For instance, fully-integrated companies, including farming,
(overall) survival to different diseases, average ge- cooperative breeding organizations, or other producer or-
netic gains varied from 4.9 to 19% in different fish ganizations may allow for a longer-term investment per-
species and white shrimp (reviewed by Gjedrem and spective than specialized breeding companies marketing
Rye, 2016). However, the limited adoption of breeding roe and fry because they usually need to be competitive
programs in aquaculture (< 10% of production based also in the short-term market situation. In the phase of
on selective breeding programs) is a major concern establishing new breeding programs that are important
(Gjedrem, 2012). The use of genetically-improved for food security, but less attractive for private investors,
stocks in aquaculture has been very low, meaning that there might be a need for public involvement. This is of-
the majority of global aquaculture production are pro- ten not straightforward and, therefore, there is a need for
duced from cultivation of wild stocks or poorly-man- research to support the development of appropriate busi-
aged broodstock without control of inbreeding rate. ness models of aquaculture breeding.
 Breeding for resilience to climate change 1809

Thus policymakers and governance should pro- uisite to apply genomic information for further genetic
vide incentives to boost selective breeding programs improvement of aquaculture production. Hence, stake-
in aquaculture for more robust farmed fish tolerating holders should support the adoption and development
climatic changes. of selective breeding by disseminating genetically-
improved materials and knowledge of selective breed-
Roles of Farming Management ing at all levels of the aquaculture sector worldwide to
ensure food security for the growing human population
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