Review: Genetic selection of high-yielding dairy cattle

toward sustainable farming systems in a rapidly

changing world
L.F. Brito, Nicolas Bédère, Frédéric Douhard, H.R. Oliveira, Mathieu Arnal,
F. Peñagaricano, A.P. Schinckel, C.F. Baes, F. Miglior

To cite this version:

L.F. Brito, Nicolas Bédère, Frédéric Douhard, H.R. Oliveira, Mathieu Arnal, et al.. Review: Genetic
selection of high-yielding dairy cattle toward sustainable farming systems in a rapidly changing world.
Animal, 2021, 15 (1), pp.100292. �10.1016/j.animal.2021.100292�. �hal-03292029�

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 Animal 15 (2021) 100292

Contents lists available at ScienceDirect

Animal
The international journal of animal biosciences

Review: Genetic selection of high-yielding dairy cattle toward

sustainable farming systems in a rapidly changing world
L.F. Brito a,⇑, N. Bedere b, F. Douhard c, H.R. Oliveira a,d, M. Arnal c,e, F. Peñagaricano f, A.P. Schinckel a,
C.F. Baes d,g, F. Miglior d
a
Department of Animal Sciences, Purdue University, 270 S. Russell Street, West Lafayette, IN 47 907, USA
b
INRAE, Institut Agro, PEGASE, 35 590 Saint-Gilles, France
c
GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326 Castanet Tolosan, France
d
Centre for Genetic Improvement of Livestock, Department of Animal Biosciences, University of Guelph, 50 Stone Road East, Guelph, Ontario N1G 2W1, Canada
e
Institut de l’Elevage, Chemin de Borde Rouge, 31 326 Castanet-Tolosan cedex, France
f
Department of Animal and Dairy Sciences, University of Wisconsin-Madison, Madison, WI 53 706, USA
g
Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern 3 000, Switzerland

a r t i c l e i n f o a b s t r a c t

Article history: The massive improvement in food production, as a result of effective genetic selection combined with
Received 17 October 2020 advancements in farming practices, has been one of the greatest achievements of modern agriculture.
Revised 18 January 2021 For instance, the dairy cattle industry has more than doubled milk production over the past five decades,
Accepted 19 January 2021
while the total number of cows has been reduced dramatically. This was achieved mainly through the
Available online 20 July 2021
intensification of production systems, direct genetic selection for milk yield and a limited number of
related traits, and the use of modern technologies (e.g., artificial insemination and genomic selection).
Keywords:
Despite the great betterment in production efficiency, strong drawbacks have occurred along the way.
Animal welfare
Genetic improvement
First, across-breed genetic diversity reduced dramatically, with the worldwide use of few common dairy
High-yielding dairy cow breeds, as well as a substantial reduction in within-breed genetic diversity. Intensive selection for milk
Resilience yield has also resulted in unfavorable genetic responses for traits related to fertility, health, longevity,
Sustainability and environmental sensitivity. Moving forward, the dairy industry needs to continue refining the current
selection indexes and breeding goals to put greater emphasis on traits related to animal welfare, health,
longevity, environmental efficiency (e.g., methane emission and feed efficiency), and overall resilience.
This needs to be done through the definition of criteria (traits) that (a) represent well the biological
mechanisms underlying the respective phenotypes, (b) are heritable, and (c) can be cost-effectively mea-
sured in a large number of animals and as early in life as possible. The long-term sustainability of the
dairy cattle industry will also require diversification of production systems, with greater investments
in the development of genetic resources that are resilient to perturbations occurring in specific farming
systems with lesser control over the environment (e.g., organic, agroecological, and pasture-based,
mountain-grazing farming systems). The conservation, genetic improvement, and use of local breeds
should be integrated into the modern dairy cattle industry and greater care should be taken to avoid fur-
ther genetic diversity losses in dairy cattle populations. In this review, we acknowledge the genetic pro-
gress achieved in high-yielding dairy cattle, closely related to dairy farm intensification, that reaches its
limits. We discuss key points that need to be addressed toward the development of a robust and long-
term sustainable dairy industry that maximize animal welfare (fundamental needs of individual animals
and positive welfare) and productive efficiency, while also minimizing the environmental footprint,
inputs required, and sensitivity to external factors.
Ó 2021 The Author(s). Published by Elsevier B.V. on behalf of The Animal Consortium. This is an open
access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

⇑ Corresponding author.
E-mail address: [email protected] (L.F. Brito).

https://doi.org/10.1016/j.animal.2021.100292
1751-7311/Ó 2021 The Author(s). Published by Elsevier B.V. on behalf of The Animal Consortium.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Implications Since the early stages of cattle domestication (~10 000 years
ago), differential selection processes have resulted in the develop-
Genetic selection is the main pillar sustaining continued and ment of about 1 200 cattle breeds (FAO, 2015) with distinct char-
incremental improvements in milk production in dairy herds, acteristics such as milk yield level, milk composition,
which is paramount for supplying nutritious dairy products for a environmental adaptation, coat color, body size, fertility, and over-
growing market. The increase in productivity has been accompa- all resilience. Currently, ~95% of the high-yielding dairy cows
nied by an alarming loss of genetic diversity, unfavorable genetic raised in the main dairy producing regions around the globe are
responses in multiple correlated traits, and reduced selection pres- represented by only three breeds: Holstein (or Holstein-Friesian),
sure in traits related to environmental efficiency, animal health Jersey, Brown Swiss, and their crosses. The worldwide spread of
and welfare, and overall resilience in comparison to performance these few breeds is mainly due to their greater milk production
traits. In this paper, we discuss the role of genetic selection in levels and responsiveness to high-input production systems. In
high-yielding dairy breeding schemes and potential routes toward these breeds and even for less common ones, both overall and
the development of more sustainable dairy cattle farming systems. per animal production levels are still rising (Fig. 2). The main dri-
vers for this increase in milk productivity are related to the indus-
trialization of dairy production; growing demand from worldwide
Introduction consumers where large industries with high export and processing
capacities (advanced infrastructure to transport and store large
Sustainable agriculture is paramount to address the major chal- amounts of dairy products) urge dairy farmers to be increasingly
lenges facing humankind, including human demography and food competitive. As a result, the increase in the overall milk production
security, climate change, energy use, biodiversity, and the environ- of many industrialized or developing countries has been accompa-
mental footprint of human activity. The current world population nied by a reduction in the total number of dairy farms and cows,
of 7.5 billion is expected to reach 9.8 billion people by 2050 and consequently, larger herds are becoming more common in
(FAO, 2020). Human diets need to become healthier, more diversi- these countries (e.g., United States and China; FAOSTAT, 2020).
fied, and better distributed across geographical regions and fami-
lies with divergent economic incomes, as there are over 690 Intensification of dairy production systems
million undernourished people in the world (FAO, 2020) and obe-
sity is rising in many regions across the globe. In this context, dairy The development of intensive dairy systems has been fueled by
products and ruminant meat provide essential amino-acids, miner- a consistent flow of innovations and technological breakthroughs,
als (calcium, zinc, selenium), and vitamins (A, B3, B6, B12, D), high- among which conventional genetic selection played a major role
lighting the fundamental importance of dairy farming for human over the past decades (Miglior et al., 2017). Animal breeding and
agri-food systems. genetics has been extensively conceptualized in artificial and stan-
There are currently more than 270 million dairy (or dual- dardized environments, where the linear equation: P (observed
purpose) cows in the world, with a global average milk yield of phenotype/performance) = G (additive genetic merit) + E (environ-
around 2 600 kg/cow/year. However, only 33 countries have a mental effects) proved to be highly efficient, especially under con-
national average milk yield greater than 6 000 kg/cow/year trolled environmental conditions and high-input production
(FAOSTAT, 2018; Fig. 1), which represents only a small fraction systems. However, when not accounting for the interactions
(~13%) of the world dairy cattle population but more than 40% of between genotype and environment (also termed Genotype-by-
the total world milk. Yet, the strong focus of the dairy industry environment interactions (GxE)), selection for high-producing ani-
on ensuring food security through higher productivity raises con- mals depends on the availability of high-quality (and usually well-
cerns on other sustainability dimensions (Clay et al., 2020). This controlled) environments for the expression of the traits of inter-
requires us questioning continued selection strategies for milk est. Indeed, together with genetic selection, the dairy industry
yield in populations (or countries) that have reached very high pro- has also benefited from major advancements in nutritional prac-
duction levels, but simultaneous selection for productivity and tices, precision management, wide adoption of reproductive tech-
functional traits (e.g. adaptation, welfare, resilience) should be nologies (e.g., artificial insemination, embryo transfer, sexed
applied in low-producing populations, especially in local breeds semen), and precision health and care management. These
and developing-country populations. advancements are not independent from each other and it is clear

Fig. 1. Distribution of countries according to their national average dairy cattle milk yield (t/cow/year). Data source: FAOSTAT, 2020.

2
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Fig. 2. Average 305-d lactation milk yield (kg) in dairy cattle breeds in Canada (thicker lines indicate the main worldwide dairy breeds). Data source: Canadian Dairy
Information Centre, 2020 (www.dairyinfo.gc.ca).

that many of them have increased the effectiveness of genetic consequently motivated the development of more efficient breed-
selection for increased productivity. From this perspective, the ing strategies for increased long-term sustainability of the dairy
high-producing dairy cow is thus more than the simple result of cattle industry (Von-Keyserlingk et al., 2013; Cole and VanRaden,
high genetic merit for key biological mechanisms and adequate 2018). Yet, to contribute to dairy farm sustainability, genetic selec-
environmental factors; it also reflects complex positive feedback tion needs to consider its direct and indirect effects on the multiple
between these two components that took place during the indus- sustainability dimensions. In our view, the extent to which the
trialization and intensification of dairy production. dynamics of genetic specialization are interrelated with dairy farm
Genetic selection for increased milk yield has been a key driver intensification is key to address the contribution of genetic selec-
of dairy intensification leading to the development of highly spe- tion to the development of sustainable production systems. In this
cialized milk production systems, with increasing herd size, and context, dairy industry stakeholders will continue seeking alterna-
heavily relying on cereals and protein-sources (FAO, 2006). Locally, tives to further increase the profitability and sustainability of dairy
the concentration of intensive dairy farms can have a large environ- production. Key players such as breeding companies and national
mental impact due to the large amounts of waste produced. Thus, genetic evaluation systems will continue refining the selection
there is growing evidence that uncoordinated levels of intensifica- indexes used in face of emerging threats and opportunities. How-
tion in high-input dairy production systems are not sustainable ever, in some cases, there might be a need for greater governmental
(Willett et al., 2019; Clay et al., 2020). Despite the major signs of involvement to support changes in certain directions, especially
progress in productivity, the long-term success of the dairy industry toward better animal welfare and environmental footprints, as well
depends on the adoption of more sustainable breeding goals and exemplified by policies implemented in some European countries.
management practices, especially from an agroecological perspec-
tive (Phocas et al., 2016a and 2016b). Current high-producing sys-
Objectives: High-yielding dairy cows for sustainable farming systems
tems need to be refined with a greater focus on animal health and
welfare, environmental efficiency, climatic adaptation, and more
The main objective of this paper is to discuss the potential con-
preparedness for future challenges through the conservation of a
tribution of genetic selection in the high-producing dairy cow
diverse genetic pool. Some breeding programs have recently
given the close relationship between genetic specialization and
included several of these traits in the breeding goals, but there is
dairy farm intensification. We first highlight the importance of
still a need for substantial improvements. For a review of the cur-
selection for milk yield (and related variables) as the driver of dairy
rent worldwide selection indexes, please see Cole and VanRaden
farm intensification and its sustainability from the single perspec-
(2018). As an example, US selection indexes include traits such as
tive of genetics. We then question the ability of the farm environ-
health, SCS, livability, productive life, feet and leg traits, and calving
ments to keep up with genetic trends. Given the genetic
ability (CDCB, 2020). The transition toward lower-input (with
background of sustainability-related traits as well as recent
improved usage of resources) production systems also needs to be
advances in genetic and genomic selection, we discuss how breed-
favored. This is required to minimize the environmental footprints
ing programs and the management of genetic resources could favor
of the industry, meet the food demands of a steadily growing pop-
the developments of more sustainable dairy systems. Finally, from
ulation in face of rapid scientific and technological innovations, lim-
the description of alternative production systems, we present pro-
ited resources and land availability, greater environmental and
spects for future research in the field of genetics of high-producing
ethical awareness of animal husbandry practices, demand for
dairy cows.
higher-quality products produced with lower use of antibiotics,
and natural challenges (e.g., new pathogens and diseases, climate
change). The role of genetic selection in non-economic dimensions Selection for milk yield as an intensification driver
of dairy farm sustainability has mainly concerned animal welfare.
However, unfavorable genetic relationships among traits of great Over the past centuries, milk production and composition were
relevance to the industry (e.g., milk yield and fertility or welfare) the main selection goals in dairy cattle breeding programs (Miglior
have deteriorated some economically important traits, which has et al., 2017) and, as a consequence, milk yield has increased dra-
3
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

matically (Fig. 2). From an economic perspective, the success of dairy cattle breeding programs over the past two decades has also
selection for increased milk yield or improved feed efficiency in contributed to a much faster rate of inbreeding accumulation per
high-producing dairy cows primarily stems at the animal level year (Makanjuola et al., 2020b).
from the dilution of maintenance requirements with increasing As previously indicated, much lower selection intensity has
production levels (Vandehaar, 1998; Brito et al., 2020a). The eco- been placed in local breeds, especially because the industry has
nomic return from increased milk yield has been the main pillar economically supported (paid for) a reduced set of production out-
for continuing genetic selection for higher milk yield. Moreover, comes (e.g., milk yield and fat/protein composition). Consequently,
greater milk yield is often considered as a key solution to address selection for a limited number of traits combined with reduced
the global challenges of ensuring food security and reducing green- population size (number of breeding animals; and consequently,
house gas emissions, as the dilution of maintenance results in both effective population size) have further increased inbreeding levels.
better feed efficiency and reduced methane emissions per kg of Selection for a larger number of traits (combined with strategies to
milk produced (Capper et al., 2009). Improvements in efficiency minimize inbreeding such as optimal contribution selection;
at the animal level alone will not necessarily result in mitigation Meuwissen, 1997) is expected to contribute for minimizing the
of global effects (e.g., methane emission) if there is an absolute rates of inbreeding as a greater set of animals could have similar
increased requirement of inputs at the farm scale. Although pro- genetic merit based on a more complex selection index in compar-
gress in milk yield depends on the farm environment, there is no ison to selection for a reduced number of traits. Therefore, when
evidence that it has been or will be genetically limited (Hill, 2016). implementing breeding programs in local breeds, it is important
to maintain a large enough breeding population and develop selec-
tion indexes that emphasize a broader range of traits. In addition,
Inbreeding levels key industry stakeholders (and potentially governmental agencies)
should reinforce the use of techniques to minimize inbreeding
Population genetic diversity is paramount for the long-term such as the use of optimal contribution selection (Meuwissen,
success of the dairy industry, as genetic progress depends directly 1997).
on genetic variability. Furthermore, reduced genetic diversity (e.g.,
allelic losses and greater inbreeding levels) has strong negative
effects on productive and reproductive efficiency, health, survival,
and overall resilience (Makanjuola et al., 2020a). Low-genetic- Depletion of genetic variation
diversity populations are also less suitable to respond to biological
threats in future unforeseen circumstances such as new pathogens From a genetic point of view, evidence for selection limits to
or environmental pressures. The main factors that have increased daily milk production is thought to be limited, especially when
the rates of genetic diversity loss are: intensive selective breeding genomic selection enables a better assessment of Mendelian sam-
for a limited number of traits, genetic drift, intensification of pro- pling and a shorter generation interval in dairy breeding schemes.
duction systems (lower animal dependency on external environ- However, depletion of genetic variation in milk yield seems unlike
mental factors), progeny testing of a limited number of bulls (Hill and Bünger, 2004; Hill, 2016), but it can happen (as observed
(prior to the genomics era), adoption of a small number of breeds in other animal species). This is likely due to the highly polygenic
worldwide (and limited, if any, investments in genetic selection nature of milk yield and other traits of interest. Furthermore, as
in local breeds), and globalization of breeding programs (e.g., use selection indexes reduce the emphasis on milk yield to simultane-
of semen from common bulls across the whole world). The rates ously select for many other important traits, greater genetic vari-
of inbreeding have increased substantially over time (Fig. 3) and ability is expected to be maintained in the long term (i.e., more
the implementation of genomic selection in the large majority of diverse genetic make-up of individual animals).

Fig. 3. Trends in inbreeding coefficients of cows from the six major US dairy breeds (thicker lines indicate the main worldwide dairy breeds). Source: Council on Dairy Cattle
Breeding (https://queries.uscdcb.com), August, 2020.

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L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Unfavorable relationships between key traits (Fig. 4b). The importance of certain reproductive traits also
depends on the production system adopted. For example, calving
Intense selection on production traits has led to unfavorable interval is less important in high-input and intensive production
correlated responses on other important traits (Rauw et al., 1998; systems, but of greater relevance in pasture-based systems (e.g.,
Rauw, 2012). These trade-offs between biological functions are Ireland, New Zealand), where greater availability of feeding
commonly interpreted under the ‘‘resource allocation theory”: resources (grasslands) need to coincide with the milk production
when two (or more) biological processes share the same resources, peaks of the herds.
they are competing in the situation of limited resources (Rendel, Health events result in substantial economic losses, including
1963). Various cases suggest that antagonistic relationships losses due to on-farm death, increased veterinary and treatment
between production traits and fitness-related traits linked to costs, premature culling, and reduced milk production (Liang
reproduction (e.g., conception rate) or health (e.g., somatic cell et al., 2017). Production and functional traits are negatively corre-
count – SCC) can be dealt with using appropriate multi-trait selec- lated, and the intense selection for milk production in the last dec-
tion methods (Berry et al., 2016; Cole and VanRaden, 2018). The ades has compromised health and fitness and increased
resource allocation theory modeling can also be applied to select environmental sensitivity (Egger-Danner et al., 2015; Friggens
for antagonistic traits, as discussed in Douhard (2013). Thus, at first et al., 2013, 2017). For instance, intense selection for production
sight, further increasing milk yield of high-producing dairy cows has led to modern high-yielding dairy cows often experiencing a
appears both desirable and possible. But situations in which lim- state of negative energy balance in early lactation, which in turn
ited resources are more likely to occur in the future because animal leads to an imbalance in metabolic processes giving rise to meta-
production systems are changing to more sustainable ones, might bolic diseases (Friggens et al., 2013). It is not surprising that
include: less control over the environment (e.g., temperature, rela- genetic correlations between milk production and metabolic dis-
tive humidity, wind speed), lower dependence on inputs (produc- eases, such as ketosis and displaced abomasum, are mostly unfa-
ing more cereals, proteins, high-quality forages, and fertilizer on vorable (Pryce et al., 2016). Traditionally, breeding programs
the farm), and the use of more preventive management strategies have focused on indirect measures of cow health and fitness, such
of health and welfare than ever before (Dumont et al., 2013; Phocas as the length of productive life or SCC as an indicator of udder
et al., 2016a and 2016b). These (extensive) systems are more health (Martin et al., 2018). However, given that direct selection
exposed to external perturbations such as a shortage of feedstuffs is more effective than indirect responses, recently many countries
that cannot be produced on the farm (e.g., by-products such as have implemented genetic evaluations for some health traits,
meals), droughts, or disease outbreaks. In this context, high- including milk fever, retained placenta, metritis, displaced aboma-
producing animals tend to be more sensitive to perturbations sum, ketosis, lameness, and clinical mastitis (Miglior et al., 2017;
(Friggens et al., 2017). Genetics of resource allocation and the Cole and VanRaden, 2018).
dynamics thereof will likely become more important in the future Heat stress is another factor negatively impacting dairy cattle
to select animals capable of maintaining different phenotypes of performance and welfare, and consequently, causing huge eco-
interest (e.g., milk production and resistance to pathogens or par- nomic losses and welfare issues to the dairy industry. Intense
asites) under challenging conditions. selection for increased production in recent decades has compro-
Genetic improvement requires sophisticated approaches, as the mised the thermoregulatory competence of dairy cows (Aguilar
large majority of relevant traits are quantitative traits and geneti- et al., 2009, Santana et al., 2017). Indeed, production and thermo-
cally intercorrelated in both favorable and unfavorable directions. tolerance are antagonistic traits because greater milk production
Therefore, sustainable breeding goals require the measurement leads to higher metabolic heat production, hence an increased
and proper weighting of all relevant traits in selection indexes to susceptibility to heat stress (Tao et al., 2020). This is alarming
enable simultaneous genetic progress in the desired direction for as global temperatures trend upward and heat waves are
all traits of interest. For instance, reproductive inefficiency results expected to become more frequent and intense. There is a nega-
in increased involuntary culling rates, increased calving intervals, tive genetic relationship between milk production under ther-
increased veterinary costs, decreased milk production, and delayed moneutral conditions and milk production under thermo-stress
genetic progress, which leads to significant economic losses for conditions (Sigdel et al., 2019). This negative genetic correlation
dairy farmers (Inchaisri et al., 2010). Production and fertility are suggests that the continued selection for greater milk yield with-
negatively correlated (Bedere et al., 2018) and therefore, selection out considering the genetic merit of the animals for thermotoler-
programs that have emphasized milk production and at the same ance will result in increasing, even more, the harmful effects of
time ignored fertility, have experienced a decline in reproductive heat stress on cow performance. Therefore, there is a critical need
performance (Royal et al., 2002; Berry et al., 2016). Fig. 4a displays for breeding for thermotolerance (Nguyen et al., 2016), which is a
the phenotypic trends in milk production and pregnancy rate in heritable trait (Ravagnolo and Misztal, 2000; Nguyen et al., 2016).
Holstein cows in the USA over the last six decades. While milk pro- Recently, the Australian dairy industry introduced a genetic eval-
duction increased markedly due to intense selection from 1960 to uation for thermotolerance which allows selection of animals that
2000, pregnancy rate declined steadily. Genetic evaluations for are more resistant to the detrimental effects of heat stress
reproductive traits were introduced in early 2000 in order to coun- (Nguyen et al., 2016).
ter the decline in cow fertility (VanRaden et al., 2004). Indeed, the
incorporation of female fertility traits into breeding programs,
together with the development of reproductive management tools, Can dairy farm intensification keep up with genetic progress?
and improvements in nutrition, health, and cows’ comfort have
significantly improved cow fertility in the last two decades. Now, Phenotypically, considerable gains in milk yield still seem
despite these advances, the reproductive performance of dairy achievable as suggested by the gap between mean production
cows remains suboptimal (Norman et al., 2018). Fig. 4b shows levels and maximum records in the recorded USA Holstein popula-
the changes in daughter pregnancy rate over time in USA Holstein tion (Fig. 5a). However relative gains of both measures decrease
cattle, in which the greater improvements seem to be in the envi- over time (Fig. 5b), similar to what has been observed for historical
ronmental components, but also a slight increase in the genetic trends of major crop yields worldwide (Grassini et al., 2013).
merit of the animals. Even using genomic information, it will take Although the phenotypic increase in average milk yield is well-
several generations to restore the initial genetic merit for the trait supported by a continuous genetic trend, improvements in farm
5
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Fig. 4. (a) Concomitant changes in milk production (lbs = pounds) and pregnancy rate (%) in US Holstein cattle in the last six decades. (b) Trends in phenotypic (P) average
daughter pregnancy rate of the recorded US Holstein population, and its genetic (G) and residual (E) components. Values are reported relative to those from 1957. Data
source: Council on Dairy Cattle Breeding website (July 2020; www.uscdcb.com).

environments in the past two decades have not kept up and may successive increments in milk yield so that the most productive
become a constraint (Fig. 6). herds are already close to milk production levels beyond which
The modern high-producing dairy cow achieves greater levels of no further gain in efficiency would be expected.
production per unit of digested feed, but higher rates of feed intake As suggested by Clay et al. (2020), it is paramount to consider
have apparently favored a long-term decline in digestive efficiency how the effects of intensification can occur synergistically (e.g.,
(Potts et al., 2017). As pointed by Vandehaar et al. (2016), the livelihoods and environment can be simultaneously improved or
importance of the dilution of maintenance effect decreases with worsened) or as trade-offs (e.g., enhanced economic efficiency

6
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Fig. 5. Trends in average milk yield of the recorded US Holstein population compared to maximum individual records (a) and the associated relative improvements between
successive measures (b). The comparison is only indicative, as data are not strictly comparable (e.g., different cow age, management). Data sources: maximum records: http://
www.holsteinusa.com/holstein_breed/breedhistory.html, and average records: https://queries.uscdcb.com/eval/summary/trend.cfm?R_Menu=HO.m#StartBody.

Fig. 6. Trends in phenotypic (P) average milk yield of the recorded US Holstein population (as reported in Fig. 5a from 1971), and its genetic (G) and residual (E) components.
Values are reported relatively to those from 1957. Data source: https://queries.uscdcb.com/eval/summary/trend.cfm?R_Menu=HO.m#StartBody.

may come at the expense of human health; Clay et al., 2020). The individual for each trait under selection, based on their economic
larger adoption of precision technologies and accumulated knowl- value or desired genetic gains (Byrne et al., 2016; Cole and
edge in multiple scientific fields (e.g., nutrition, reproductive man- VanRaden, 2018). Selection indexes have been refined over time
agement, soil sciences, water management, agroecology, grassland to enable direct breeding emphasis toward specific production sys-
management, ambiance control) also support the development of tems, market demands, or to address emerging production, envi-
tools to enable optimal phenotypic expression of the genetic merit ronmental, or societal aspects of the dairy industry and society
of animals raised in different dairy production systems. as a whole (Cole and VanRaden, 2018). Frequently, economic val-
ues in the breeding objectives are the key inputs to cost–benefit
Developments in dairy cattle genetic evaluations analysis and optimization of breeding schemes, but in some cases,
it is challenging to define economic values for certain traits and
Since domestication, the key traits under artificial selection therefore, selection indexes tend to be constructed based on
(mainly based on phenotypic performance) were temperament desired gains or a blend of economic values and desired gains
(and other behavioral traits), physical and anatomical variables (Amer and Byrne, 2019). There are several national selection
(e.g., coat color, body size), and milk production. With the method- indexes (Cole and VanRaden, 2018) that differ based on the empha-
ological developments in the area of quantitative genetics, animal sis put in each trait category (production, reproduction, health,
breeding, and phenomics, the array of traits targeted for improve- workability, efficiency, and body conformation). However, it is
ment has expanded substantially over the past five to six decades paramount to have more differentiated indexes to meet niche mar-
as a response to the dynamic requirements of dairy producers, con- kets and alternative breeding goals (Phocas et al., 2016a and
sumers, and society in general. As multi-trait selection became the 2016b; Lopez-villalobos et al., 2018). Commercial breeding goals
norm in dairy breeding programs, the development of selection will continue to be refined regularly due to changes in production
indexes played a major role in balancing the genetic merit of each conditions, market requirements, and societal developments. Fur-

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L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

thermore, as the biological background (including genetic relation- the worldwide dairy industry depend on a plethora of factors such
ships) of novel and traditional traits is uncovered and phenotyping as the production systems (e.g., intensive, pastoral and grass-based
technologies are commonly used, more efficient selection indexes systems, mixed farming-livestock, transhumance, and small-
will be proposed (Nieuwenhoven et al., 2013). holders), geographical region, climatic conditions, management
The success of genetic evaluation schemes has been made possi- practices, cultural preferences, and market demands. In this con-
ble due to substantial advancements in statistical methods and com- text, certain breeds have evolved and become more adapted to
puting resources. The development of methods have played a major specific regions, while others are more cosmopolitan and raised
role on enabling rapid genetic progress in the main dairy cattle pop- in a wider range of production systems (e.g., Holstein, Brown
ulations. For detail reading of the genetic evaluation systems, please Swiss, Jersey, and their crosses).
see: Weigel et al. (2017), Misztal et al. (2020), and Grosu et al. (2014). Genomics information provides knowledge on specific alleles
Nowadays, the majority of genetic evaluations for dairy cattle (as and haplotypes and therefore, can be used to more accurately
well as other livestock species) are based on the Mixed Model Equa- assess genetic diversity levels, relatedness between individuals
tions (MME) and the Animal Model. In general, variance components and populations, and presence/absence of deleterious mutations
(e.g., heritability estimates) are estimated based on likelihood (e.g., (e.g., Guarini et al., 2019). The wide use of reproductive technolo-
REML – Restricted Maximum Likelihood) and Bayesian methods. gies such as artificial insemination, coupled with short generation
Globalization allowed the exchange of genetic material, such as intervals (due to the implementation of genomic selection) can
semen and embryos, which required across-country genetic evalua- speed up the multiplication and transmission of deleterious alleles
tions (MACE, Schaeffer, 2001). The discovery of major genes by across populations. In this context, genomic information should be
molecular geneticists facilitated the selection of animals with favor- better used to manage genetic diversity in dairy cattle populations
able genotypes for some important traits. However, the success of and remove deleterious mutations.
marker-assisted selection was limited by the great distance between The maintenance of high genetic diversity in dairy cattle popu-
the causal mutations and genetic markers. Thus, even though lations (within and across breeds) is crucial to prevent the situa-
advancements made over time were very important to ensure tion in which a single (or few) breeds have to fit all dairy
genetic progress, the use of genomic selection (Meuwissen et al., farming systems. In some countries, the conservation of local
2001) allowed rapid genetic progress in dairy cattle (Schaeffer, breeds has been done by using these populations for organic farm-
2006). Recently, the genomic relationship matrix (VanRaden, ing, development of special products for niche markets, and for
2008) has been combined with the traditional pedigree-based rela- new functions such as landscape and nature management
tionship matrix, in order to create a hybrid matrix that is used to (Oldenbroek, 2019). In general, small breeds are unfavored because
simultaneously generate breeding values for genotyped and non- they cannot take full advantage of genetic and genomic selection
genotyped animals, a method known as single-step GBLUP schemes (thus lower genetic progress per time unit) and there is
(ssGBLUP, Misztal et al., 2009; Aguilar et al., 2010), which has a smaller investment from the artificial insemination market, as
become a gold standard for genomic evaluations in livestock. breeding companies tend to be more interested in larger breeds
Current research efforts have focused on developing and testing (Biscarini et al., 2015). This is a major challenge that needs to be
more computationally efficient algorithms and methods to facili- addressed in the dairy industry. The maintenance of large numbers
tate the implementation of ssGBLUP in large datasets (e.g., of local-breed animals will depend on the definition of their eco-
Oliveira et al., 2019), as well as the development of alternative nomic value in face of challenging and changing conditions such
methods based on machine learning (Gengler, 2019). The use of as climate change, greater diversification of production systems
alternative data sources such as whole-genome sequence informa- (e.g., organic, pasture-based, precision farming), and increase
tion (not only additional SNP markers), structural variations, and usage of by-products and alternative feed sources. Furthermore,
high-throughput phenotyping (e.g., automated data recording sys- several local breeds have cultural and social values to certain
tems), has also received a lot of attention and might contribute to regions and are likely to be conserved as part of such traditions.
increasing the rates of genetic progress in dairy cattle. However, It is very unlikely that a single breed can perform well across a
the use of these alternative data sources is still incipient. wide range of production systems and environmental conditions.
Furthermore, intensive selection in key dairy breeds have already
Genetic trends for traits under selection caused fixation of certain alleles that might have undesirable
effects related to fitness traits in low-input production systems.
Genetic selection has been very effective in improving various Therefore, local breeds are a reservoir of genetic material to be
traits included in selection indexes in dairy cattle, as reviewed by potentially transferred to the key dairy breeds (e.g., Holstein)
Miglior et al. (2017) and Cole and VanRaden (2018). All traits under through gene editing and crossbreeding schemes. As local breeds
selection have been genetically modified over time (Fig. 7), with are already adapted to certain management and environmental
genetic gain rate depending on factors such as trait heritability challenges, it might be more economically feasible to genetically
and emphasis in the overall selection indexes. Furthermore, the improve local breeds for greater performance in these systems
implementation of genomic selection in the past decade has sub- than selecting cosmopolitan dairy breeds (e.g., Holstein) for better
stantially contributed to increment the rates of genetic progress adaptation and welfare under harsher conditions.
by increasing the accuracy of breeding values of young animals Crossbreeding is not widespread in dairy cattle, in comparison
(Fig. 8), reducing the generation interval, and evaluating a larger to other livestock species (e.g., poultry and pigs), and therefore,
number of selection candidates (in comparison to conventional within-breed genetic diversity is even more important. However,
progeny testing). in developing countries and tropical regions, crossbreeding (espe-
cially between Bos taurus taurus and Bos taurus indicus breeds)
Potential contributions of genetic selection to more sustainable has been used as an alternative to increasing productivity of local
dairy farms populations through the development of more productive and cli-
matic adapted composite breeds [e.g. Brazilian Girolando (Canaza-
Genetic resources Cayo et al., 2016)]. Recent studies have also investigated the role of
crossbreeding to mitigate inbreeding depression and genetic diver-
The development and choice of genetic resources (e.g., breeds or sity management (Dezetter et al., 2015) or on the performance and
lines) and breeding schemes (e.g., crossbreeding) implemented in profitability of dairy herds (Dezetter et al., 2017).
8
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Fig. 7. Genetic trend (based on breeding values) for various selected traits in US Holstein cows and bulls, plotted by birth year. Data source: https://queries.uscdcb.com/
eval/summary/trend.cfm. Net_merit_cows, Cheese_merit_bulls, Cheese_merit_bulls, Grazing_merit_bulls, and Fluid_merit_bulls represent selection index values for cows
and bulls as defined by the Council on Dairy Cattle Breeding (CDCB, USA). Productive_life_cows: breeding value for productive life of cows, DPR_cows: breeding value for
daughter pregnancy rate of cows, HCR_cows: heifer conception rate, CCR_cows: cow conception rate, Sire_calving_easy: breeding values for sire calving easy,
Daughter_calving_ease: breeding value for daughter calving easy, SCS_cows and SCS_bulls: breeding value for somatic cell score of cows and bulls, Fat_cows and
Protein_cows: breeding value of cows for fat and protein, respectively.

Fig. 8. Comparison of genomic and traditional PTA (Predicted Transmitting Ability) for US Holstein cattle (August, 2020). Data source: The Council on Dairy Cattle Breeding
(https://queries.uscdcb.com/eval/summary/comparexml_menu.cfm).

Moving forward, optimal contribution selection (Meuwissen, cattle breeding sector is mainly driven by private companies. In
1997), which maximizes genetic gains under constrained levels general, dairy farmers are becoming more informed of the negative
of inbreeding, should be widely adopted in both numerically large consequences of inbreeding and are implementing mitigation
and small breeds. A second alternative is to minimize inbreeding alternatives (e.g., use of mating software and assistance of exten-
while maintaining a certain rate of genetic response (Colleau sion specialists). Furthermore, we believe that governmental agen-
et al., 2004). These alternatives might be challenging as the dairy cies should reinforce the importance of maintaining genetic

9
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

diversity by discouraging mating of close relatives or designing a The role of local breeds toward increased dairy sustainability
payment system to motivate conservation of genetic diversity
within and across breeds. Diversity metrics based on genomic In general, local breeds: (1) are more adapted to less intensive
information should be assessed across multiple dairy breeds and and suboptimal management practices and harsher environmental
used for proper management of genetic resources. Lastly, consider- conditions such as high temperature and relative humidity, endo-
ing the importance of high genetic diversity for future genetic pro- and ectoparasites, higher altitudes, or lower-quality feed; (2) have
gress and adaptation to changing and challenging environments, greater fertility and longevity; and, 3) have lower incidence of
more public funds should be used to promote local genetic metabolic diseases, hoof health issues, and reproductive disorders
resources and financially support the conservation of rare or (e.g., Dillon et al., 2003a and 2003b; Walsh et al., 2007, 2008;
non-mainstream dairy breeds. Bedere et al., 2017a, 2017b and 2018). The large majority of these
traits are already under selection (or in research stages) in Holstein
Genotype-by-environment interactions (and other cosmopolitan breeds) breeding programs around the
world. However, in addition to continue selecting for these traits
In general, structured breeding programs have increased the in cosmopolitan dairy cattle breeding programs, considering the
genetic merit of dairy animals and have been accompanied by an heritability of fitness traits (e.g., health, longevity, fertility), it
improvement in the environmental conditions through manage- might be more cost-effective to genetically improve the perfor-
ment practices, both of which are needed for high productivity. mance of local breeds while also avoiding deterioration of fitness
However, there is a wide range of production systems (from exten- traits, as already observed in breeds such as Holstein. In other
sive and low-input to intensive and precision-technology farms), words, the participation of local breeds in dairy production is
and the best genotypes selected under certain conditions will not expected to increase as their production levels are improved and
necessarily perform well in other environments or production sys- adaptation and fitness are retained. On the other hand, Holstein
tems, i.e., GxE (genotype x environment). Briefly, GxE interaction (and other cosmopolitan dairy breeds) will be selected for
can be defined as a change in the response of genotypes to different increased fitness and adaptation with a reduced focus on milk
environments or changes in the relative merit of genotypes in dif- yield. At the end, both breed groups will be more adapted to play
ferent environments (Rodríguez-Bermúdez et al., 2019; Mulder, an important role in specific production systems (e.g., precision
2017). Genotype-by-environment between environments leads to farming and high-input vs low-input farming).
lower genetic gain if the selection is performed in a different envi-
ronment (e.g., a nucleus), than in which the commercial animals Novel breeding goals for long-term sustainability
are performing (Mulder, 2017). Selection for increased productivity
has also led to greater environmental sensitivity (Rauw et al., 1998; The long-term sustainability of the dairy cattle industry
Friggens et al., 2017) and therefore, it is expected that larger GxE depends on the development of balanced breeding goals to simul-
effects will be observed when high-yielding dairy cows are raised taneously improve animal health and welfare, productive effi-
in different production systems compared to those in which they ciency, environmental impact, food quality and safety while
were selected in (especially low-input systems, Dillon et al., minimizing the loss of genetic diversity. Genetic selection for some
2003a and 2003b). of these breeding goals have already been implemented around the
Over time, GxE was ignored in many instances, as the environ- world (e.g., Miglior et al., 2017; Cole and VanRaden, 2018) and cer-
ments for intensive production are mainly controlled. However, tain countries have placed greater emphasis in these novel traits,
considering the current challenges (e.g., higher average tempera- especially in Europe. The wide availability of genomic tools pro-
tures) and energy costs, there is a need to genetically select more vides a great venue to genetically improve traits that are difficult
resilient and robust animals (Mulder, 2017; Berghof et al., 2019). or expensive to measure (e.g., disease resistance, welfare, longev-
Several strategies have been sought to overcome these issues. First, ity, methane emissions) as well as to better manage genetic diver-
breeding schemes can consider GxE in genetic and genomic evalu- sity (Meuwissen et al., 2020). The refinement of breeding programs
ations to identify the most suitable genotypes for each condition. to incorporate novel breeding objectives requires the development
This can be done through the use of reaction norms using routinely of high-throughput phenotyping technologies (and structured and
recorded datasets such as milk yield and climatic variables or continuous data recording streams), investigation of the genetic
direct indicators of resilience and welfare (Berghof et al., 2019; relationship between novel traits and those routinely recorded
Brito et al., 2020b). Different tools and approaches can be adopted (and the potential consequences of selection for every single trait),
to collect phenotypes to be used for genetic selection. For instance, the performance of large-scale genomic studies, especially geno-
precision technologies (e.g., activity sensors, feeding behavior mic predictions and genome-wide association studies, and refine-
recorders, automated milking robots, computer vision) can gener- ment of selection indexes to reflect improved knowledge of
ate a wealth of data to maximize genetic progress for traits related biology, new sources of data, and changing conditions in the envi-
to resilience and welfare, as reviewed by Berghof et al. (2019) and ronment and economy (Cole and VanRaden, 2018).
Brito et al. (2020b), respectively. The greatest obstacle for including multiple traits in dairy cattle
Secondly, local breeds can be used for the introgression of desir- breeding programs has been the cost and difficulty to measure a
able alleles, crossbreeding with exotic breeds, and development of large number of animals for close-to-biology traits, which usually
new composite breeds. When animals are genetically adapted to lack well-defined phenotypes. The availability of precision tech-
specific environmental conditions or production systems, they will nologies, that can be used across multiple production systems, is
tend to be more productive, have better welfare, and production an opportunity to measure novel traits, especially resilience, wel-
costs will be lower. In addition to environmental conditions, a wide fare, and environmental efficiency (Brito et al., 2020b). Intensive
variety of production systems are becoming more common around selection for production traits combined with the intensification
the globe, including precision-technology-based dairy farms, of dairy cattle production systems has resulted in animals that
organic, and agroecological production systems. Thus, different are at greater risk of behavioral, physiological, and immunological
selection indexes need to be developed to select animals that per- disorders (Barbat et al., 2010; Colditz and Hine, 2016; Friggens
form well, have a better life (in terms of positive welfare, health, et al., 2017; Lawrence and Wall, 2014; Rauw et al., 1998, 2012;
longevity), and are part of an environmentally and economically Star et al., 2008). Therefore, key groups of novel traits are: health
sustainable production system. (e.g., udder health, hoof health, metabolic disorders), fertility, feed
10
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

efficiency, methane emissions, longevity, and overall resilience. cows (milk and meat). The meat from culled cows and calves
Additional breeding goals or differential emphasis in selection was considered to be less polluting than meat from a suckling herd
indexes are required depending on the production system. For (Puillet et al., 2012). This pattern can be improved by the use of
instance, major traits for agroecological dairy farming are: behav- female sexed semen for the renewal of the dairy herd and male
ior (feeding on new resources, well-being indicators), overall resi- sexed semen to produce well-conformed animals for meat
lience, reproduction, and nutrient efficiency. As we focus on production.
increasing dairy sustainability, it will be crucial to evaluate the ani- Rustic strains of Holstein-Friesian can be adapted for organic
mals’ efficiency to digest alternative feed sources (e.g., grasslands dairy herds as they are bred in pasture-based systems (as in New
and forages, algae, food industry by-products, local crops). Further- Zealand and Ireland; Rodríguez-Bermúdez et al., 2019). In the cur-
more, even animals with similar feed efficiency might still differ rent organic dairy herds, no strategy seems to have been adopted
with regard to manure composition (e.g., nitrogen/phosphorous massively and producers are still experimenting, using conven-
ratio), which will become increasingly important in order to miti- tional breeds, as purebreds or crossing schemes, or local breeds (-
gate the negative impact of animal production on the environment. Rodríguez-Bermúdez et al., 2019). Nauta et al. (2009) showed that
For each group of traits, related variables might also be useful indi- multifunctional organic farming (vs specialized organic dairy farm-
cators (e.g., feeding behavior and feed efficiency). Depending on ing) could adopt local dairy breed as a commercial strategy for
the production system adopted (e.g., beef-on-dairy, extensive pro- agritourism, and participate in a living gene-bank supported by
duction), beef traits (carcass, body size, meat quality) will also subsidies from the European Commission.
need to be genetically evaluated. Fertility and reproduction are of In specialized organic dairy herds, crossbreeding could be
great importance in high-yielding dairy herds, but it is even more increased. A large-scale experiment that studied several crosses
important in less specialized systems where milk production peak for more than three generations has shown that Holsteins can be
needs to overlap with the grasslands growing season. crossed with Montbeliarde, which is a dual-purpose breed with
significant muscle development and good fertility. This cross can
then be mated with Scandinavian Red, which has good health char-
Alternative options to intensive (high-input) dairy production acteristics (Hazel et al., 2020, 2021). The rotational crossbreeding
systems: The role of genetic selection between these three breeds exploits well the complementarity
across breeds. For farms that have climatic conditions that allow
There is a plethora of production systems being explored world- for year-round grazing, Montbeliarde could be replaced by Jersey
wide. As reviewed by Clay et al. (2020), sustainable intensification to have more adapted animals for grazing systems. The rotational
is related to increasing productivity while simultaneously decreas- crossbreeding seems to be more rapid than selection in pure
ing the negative environmental effects of conventional farming breeds, as it has the advantage of maintaining the heterosis effect
practices and improving animal welfare. Secondly, agricultural and suppressing inbreeding. From a genetic evaluation point of
multifunctionality provides an opportunity to derive diverse bene- view, evaluations maximizing the heterosis effect could be devel-
fits from agroecosystems that extend beyond the production of oped, as in various plants and non-ruminant breeding programs
food and fiber to include environmental services (e.g., carbon (González-Diéguez et al., 2020).
sequestration, biodiversity, and water quality) and maintenance
of social-cultural processes. Moreover, agroecology emphasizes
Conclusions
the context-specific nature of agroecosystems and considers how
ecological principles can help achieve goals of sustainability and
Remarkable achievements have been accomplished in the dairy
social equity (Clay et al., 2020). Prospective scenarios offer inter-
cattle industry over the past decades, with a massive increase in
esting insights for the development of current production systems
milk productivity (in a limited number of breeds). Unfortunately,
as they address the multiple challenges of sustainability (e.g.,
this progress has been accompanied by strong drawbacks, includ-
impacts of diets on health, food security, climate change, biodiver-
ing loss of genetic diversity and deterioration of key biological
sity loss) in a systemic view. Achieving sustainability in its multi-
mechanisms (e.g., health, resilience, robustness, welfare, longevity)
ple dimensions is extremely ambitious and complex given that
in the most common dairy cattle breeds. Moving forward, the
actions on a particular dimension may be detrimental to another
development of a more sustainable dairy cattle industry will
dimension. In scenarios emphasizing profound transitions toward
require continued innovations in multiple areas, especially in
agroecological systems, there is a very large reduction in farm
genetics, strong involvement of all stakeholders (e.g., farmers,
inputs and associated with a reduction in yield. In the case of dairy
technical and scientific sectors, consumers, policy-makers), diver-
production systems, for instance, the TYFA model developed at
sification of production systems, and great support from govern-
European scale (Poux and Aubert, 2018) includes two typical dairy
ments and private institutions toward experiencing and
systems in 2050:
developing alternative production systems. There seems to be a
consensus on the need to continue refining the current selection
(i) ‘‘a grass-fed system, in which the majority of fodder resources
indexes and breeding goals to incorporate or give greater emphasis
come from permanent grasslands, with an average level of pro-
on traits related to animal welfare, health, resilience, longevity, and
ductivity per cow of 5 000 kg of milk/year” and,
environmental efficiency. Novel phenotyping technologies, closer-
(ii) ‘‘a mixed system, in which permanent grasslands are combined
to-biology traits, and genetic and genomic evaluation methods will
with other fodder resources: temporary grasslands, cereals, and
continue to be developed and should be addressed to specific pro-
legumes (alfalfa, clover). The average production level is 7
duction systems. Finally, genetic selection of high-yielding dairy
000 kg of milk/year”.
cattle will need to be part of more systemic approaches at the farm
scale to favor profound transitions toward sustainable farming
Similarly, the Afterres2050 scenario developed at the French
systems.
scale (Couturier et al., 2017) suggests the progressive replacement
of high-input dairy systems (i.e., with milk yield average >10
000 kg/year/cow) by low-input systems with more moderate pro- Ethics approval
duction levels. In both scenarios, the dairy herd replaced the beef
herd and the less specialized dairy cow were also dual-purpose Not applicable.
11
L.F. Brito, N. Bedere, F. Douhard et al. Animal 15 (2021) 100292

Data and model availability statement strategies for improvement. The Journal of Reproduction and Development 56,
S15–S21.
Bedere, N., Disenhaus, C., Ducrocq, V., Leurent-Colette, S., Delaby, L., 2017a. Ability
None of the data were deposited in an official repository. All the of dairy cows to be inseminated according to breed and genetic merit for
data used in this review are publicly available in the tables and production traits under contrasting pasture-based feeding systems. Animal 11,
826–835.
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Bedere, N., Disenhaus, C., Ducrocq, V., Leurent-Colette, S., Delaby, L., 2017b. Ability
of dairy cows to ensure pregnancy according to breed and genetic merit for
Author ORCIDs production traits under contrasted pasture-based systems. Journal of Dairy
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Bedere, N., Cutullic, E., Delaby, L., Garcia-Launay, F., Disenhaus, C., 2018. Meta-
Luiz F. Brito: https://orcid.org/0000-0002-5819-0922 analysis of the relationships between reproduction, milk yield and body
N. Bedere: https://orcid.org/0000-0002-7382-9309 condition score in dairy cows. Livestock Science 210, 73–84.
Berghof, T.V.L., Poppe, M., Mulder, H.A., 2019. Opportunities to improve resilience in
H.R. Oliveira: https://orcid.org/0000-0002-0355-8902 animal breeding programs. Frontiers in Genetics 9, 692.
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A. P. Schinckel: https://orcid.org/0000-0002-8614-7198 and opportunities in genetic improvement of local livestock breeds. Frontiers in
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F. Miglior: https://orcid.org/0000-0003-2345-8842 Brito, L.F., Oliveira, H.R., Houlahan, K., Fonseca, P.A.S., Lam, S., Butty, A.M., Seymour,
D.J., Vargas, G., Chud, T.C.S., Silva, F.F., Baes, C.F., Canovas, A., Miglior, F.,
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Author contributions feed utilization and implementation of genomic selection for improved feed
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587–604.
Luiz F. Brito: Conceptualization, Methodology, Writing - Origi- Brito, L.F., Oliveira, H.R., McConn, B.R., Schinckel, A.P., Arrazola, A., Marchant-Forde,
nal Draft, Visualization, Project administration, Writing - Review J.N., Johnson, J.S., 2020b. Large-scale phenotyping of livestock welfare in
and Editing, Nicolas Bedere: Conceptualization, Methodology, commercial production systems: a new frontier in animal breeding. Frontiers in
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Writing - Original Draft, Visualization, Writing - Review and Edit- Byrne, T.J., Santos, B.F.S., Amer, P.R., Martin-Collado, D., Pryce, J.E., Axford, M., 2016.
ing, Frederic Douhard: Conceptualization, Methodology, Writing New breeding objectives and selection indices for the Australian dairy industry.
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Canaza-Cayo, A.W., Cobuci, J.A., Lopes, P.S., Torres, R.A., Martins, M.F., Daltro, D.S.,
Hinayah R. Oliveira: Methodology, Writing - Original Draft, Writ-
Silva, M.V.G.B., 2016. Genetic trend estimates for milk yield production and
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production: 1944 compared with 2007. Journal of Animal Science 87, 2160–
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F. Baes: Writing - Review and Editing, Filippo Miglior: Conceptu- alternatives. Ambio 49, 35–48.
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Changes in animal performance and profitability of Holstein dairy operations
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