Development of genetically improved tropical-adapted dairy cattle

Abstract

Limited animal production undersupplies animal-sourced foods to populations in tropical regions while improving local productivity promotes food security and livelihoods. Strategically exploring traits of interest from distinct genetic groups is a valuable tool to promote the sustainability of livestock systems. Genetic improvement of animals requires well-structured programs to avoid the opposite effect. When developing these programs, a broad approach should be considered that ideally accommodates the local necessities and conditions where they are being implemented. According to recent estimates, about 80% of cattle reside in tropical or subtropical regions (Cooke et al., 2020a). The number of farmers and consumers, as well as overall production (e.g., annual milk production), is also greater in the tropics. However, cattle productivity in these regions is underwhelming compared with most temperate zones characterized by high-input farming practices and yields correlated with the fitness of the breeds to their system. Furthermore, it results from the adverse conditions derived from the underprivileged economic, social, and climatic conditions of the region (Oosting et al., 2014). Therefore, although livestock activity is broadly represented in the tropics, many challenges must be overcome to achieve sustainable production systems that meet this crucial demand, mostly among low-income smallholders. According to the World Bank (World-Bank, 2007), the necessity for increased productivity in the tropics arises from three different demands. One of them is the insufficient availability of animal-sourced foods decreasing protein and essential nutrients (i.e., vitamin B-12 and fatty acids) supplies, which are predominant elements of undernutrition (Guiné et al., 2021). It also results from environmentally unsustainable animal production practices, inappropriate land use, and its influence on climate change. Finally, the state of deficient livelihoods, as many people rely on farming exclusively. The aspects mentioned above are englobed in a sustainable food system (SFS), described by FAO (2018) as “a food system that delivers food security and nutrition for all in such a way that the economic, social and environmental bases to generate food security and nutrition for future generations are not compromised,” which relates to a universal approach to food security matters. There are several prospects for promoting SFS, and excellent results are described by the introduction of straightforward management practices. For example, Oosting et al. (2014) separated dairy cattle feed into ten classes, “1” being greatest quality and “10” being least quality, to compare herd performance. Overall, offering a greater-quality ration improves the average milk production per animal, reducing methane emissions per kilogram of milk. However, the greatest quality ration offer did not yield optimal herd milk, probably because the diet failed to meet the distinct requirements of the animal. Their findings suggest a critical relationship between genetic characteristics and nutritional value and amount of feed, supported by O’Neill et al. (2010) that describes the “complex interactions between genotype, environment, and management (G × E × M)” and its connection with the performance of an animal. To supply this demand, our research group and collaborators are developing genetics focusing on particular environmental conditions in locations within the tropics. We aim to introduce more efficient animals, develop and promote progressive farming techniques, optimizing the positive effects described in the previous paragraph, as well as other production traits. We will establish these herds based on the strategic exploration of traits of interest identified in different cattle genetic groups (Bos taurus and Bos indicus). This strategy has shown excellent production potential in the tropics (Cooke et al., 2020b; Vieira et al., 2022). Distinct breeds will be utilized, primarily focusing on dairy but likely expanding to the beef sector, using a similar approach, addressing the needs of smallholder farmers. The project emphasizes nutrition and livelihood improvement mainly by increasing animal-sourced food availability and the income of the farmer through more sustainable livestock systems. However, besides food supply, food security relies on adequate regulatory measures and political consistency (Guiné et al., 2021), the ultimate components of the panorama of the project. Bos taurus taurus has been naturally selected and evolved to suit the temperate climate. In addition, as they were raised and selected by different social groups, breeds diverged to distinct body sizes (large and medium) and purposes (dairy, beef, dual purpose). Some examples of taurine cattle of different sizes and aptitudes are Charolais (large, beef), Jersey (medium, dairy), and Normande (medium, dual purpose). In addition to these local conditions, the evolution of their traits is marked by global industrialization, which increases the demand for animal-origin products. Therefore, these modern breeds have undergone extensive artificial selection and controlled breeding practices, targeting greater production capacity phenotypes (O’Neill et al., 2010). Inevitably, it increased inbreeding levels (Purfield et al., 2012) and the incidence of undesired recessive alleles, resulting in detrimental effects on functional traits like fitness, longevity, and reproduction (Rauw et al., 1998). For these reasons, current breeding programs are coordinated using genotypic information to deviate from it. European taurines are animals with high input, excellent production capacity, and high susceptibility to stressors of the tropics. Unlike taurines, B. taurus indicus cattle, originally from India (Naik, 1978), evolved from tropical and more challenging environments, acquiring unique endurance characteristics. As a result, they present an increased capacity for maintaining body temperature in high heat conditions and overcoming parasite challenges. In addition, a reduced metabolism and maintenance requirement added to the ability in digesting inferior quality fodders (Hunter and Siebert, 1985). These traits allow them to sustain their performance (e.g., reduced pregnancy loss) even under restricted nutritional conditions (Fontes et al., 2019). B. indicus animals are called indicine, humped, or zebu cattle and represent about 75 breeds, for example, Gir, Guzerat, Kangayam, and Nelore. Currently, because of indicine suitability to stressful environments, these breeds have spread around subtropical and tropical countries for beef, dairy, and draft purposes (Turner, 1980; Madalena, 2002). However, they show limited productive potential even after artificial selection, compared with taurine animals under optimal conditions (Turner, 1980). In tropical conditions, taurine cattle are more susceptible to diseases and metabolic disorders, failing to express their productive potential while indicine cattle are not able to sustain satisfactory production. However, as the subspecies evolved, they acquired particular traits of interest as tropical-adapted livestock (Figure 1). While B. taurus show high production potential (beef and dairy), feed conversion efficiency, and reduced age at first calving, B. indicus have greater longevity and high heat, disease, and parasite resistance. When combined, these traits generate the ideal tropical-adapted animal. Widespread crossbreeding of B. taurus and B. indicus cattle is a valuable strategy to accomplish that. Representation of B. taurus (taurine) and B. indicus (indicine) cattle. Associated to their corresponding climatic and geographic regions of origin and traits of interest for tropical-adapted cattle crossbreeding. Background map courtesy of https://ian.macky.net/pat/license.html. The descendants of purebred crosses are expected to perform better than their ascendants because of the separation of unfavorable alleles (Sørensen et al., 2008). Additionally, the more distinct the parental breeds are, the more significant the heterosis or hybrid vigor impact, which is the case of B. taurus × B. indicus. The hybrid vigor influence is predominantly detected in health, longevity, and reproduction. However, it will also affect advantageous genetic arrangements observed in the founder breeds (Falconer and Mackay, 1996). Hence, for successful crossbreeding results, a tactical determination of breeds and genes of interest is critical, besides an extensive application of genomic information to guide purposeful matings. A few of the composite/synthetic dairy breeds that were developed by crossbreeding B. taurus and B. indicus breeds are listed in Table 1. Dairy Composite Breeds that were previously developed by crossbreeding B. indicus and B. taurus breeds As previously mentioned, the objective of the breeding programs was to produce offspring that would carry the relative strengths of the B. taurus and B. indicus founder breeds. Development of composite breeds was no easy task, sometimes consuming many decades. Nevertheless, in the successfully concluded programs, the crossbreds manifested the desired traits. On the one hand, they exhibited superior milk production and fertility traits compared with their B. indicus ancestors. On the other hand, compared with their B. taurus ancestors, they showed superior heat tolerance and parasite resistance in the tropics. For example, AMZ and AFS cows have often produced in excess of 6,000 liters/lactation under tropical Australian conditions. This milk production is more than double the typical lactation yields of their B. indicus ancestors. Tick resistance among crossbreds has also been reported (e.g., number of ticks on crossbreds was <10% of that in purebred taurines; Madalena, 2002). Unfortunately, in many crossbreds, F2 and F3 generations did not perform as well as their parents (F1). For example, in Thailand, Malaysia, and India, these crossbreds failed to produce more than 2,000 liters/lactation (Clarke and Sivasupramaniam, 1983; Umpaphol et al., 2001). According to some studies, the F2 generation also performed poorly with certain reproductive traits like age at first calving and calving interval compared with the F1 generation (Syrstad, 1989; McDowell et al., 1996). Reviewing the status quo of each composite breed is beyond the scope of this article. However, one point needs to be emphasized; many of these crossbreeding programs have ceased functioning today. Underlying reasons are numerous, underperforming offspring being an obvious one. Going against the grain, one composite breed in particular, namely the Girolando, has risen above the rest and flourished, particularly in Brazil. The hybrid has succeeded so much in Brazil that in 2021, about 80% of the total milk production of the country’s 35 billion liters (IBGE, 2021) came from Holstein × Gyr crossbreds (Silva et al., 2022). The first crossbreeding happened over 80 years ago in Brazil. Soon, many farmers started adopting this strategy, and extension programs developed. However, progeny testing began only in the 1990s, through joint efforts of the Brazilian Association of Girolando Breeders and Brazilian Agricultural Research Corporation (Embrapa). Later, these companies implemented the Program of Genetic Improvement of Girolando (PMGG) for a more resourceful and embracing approach. The program aims to detect and propagate outstanding genetics to stimulate Brazilian dairy sector sustainability. As a result, in 20 years (2000–2021), a 63% increase (3,695 kg to 6,032 kg) is reported for the average production of a Girolando in 305 days (Silva et al., 2022). Nowadays, Brazil is the fifth largest milk producer in the world (FAO, 2021). The achievements of the Girolando project arise from well-established strategies and intensive efforts. According to Silva et al. (2022), the PMGG collects and processes genotypic, phenotypic, and pedigree data from thousands of local farms. It uses molecular markers to identify alleles of interest in milk production, like volume, protein profile, fat content, and genetically inherited disorders. In addition, it develops and applies several analyses and indexes for morphological, reproductive, and productive characteristics, such as Girolando Tropical Efficiency Index (IETG), which incorporates information about animal longevity and heat stress tolerance (Silva et al., 2022). Moreover, the index categorizes animals by their capacity to sustain productivity in tropical conditions. Considering all these available tools, farmers can assertively select and maintain efficient animals in their herds and plan for strategic matings. Girolando cattle comprises animals of distinct genetic groups according to the proportions of the founder breeds (H (dam) × G (sire)). For example, 1/4H, representing a bovine that is 1/4H, 3/4G, and other common assemblies like 3/8H, 1/2H, 5/8H, 3/4H, and 7/8H. Although the heterozygosis effect is present in all cross levels, they may present distinct attributes and responses to environmental conditions. Vieira et al. (2022) analyzed records from 1,221 Girolando herds in southeast Brazil (tropical Atlantic climate) composed of different Holstein and Gyr proportions. They found that 1/2H, 3/4H, and 7/8H animals perform similarly better in production and reproduction than 1/4H and 3/8H. Corroborating with these findings, da Costa et al. 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