Inbreeding analysis of the population of Holstein cattle registered in the Official Milk Control System of Argentina

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1 ARTICLES RIA / Vol. 43 / N.º 1 Inbreeding analysis of the population of Holstein cattle registered in the Official Milk Control System of Argentina ABSTRACT Increasing values of inbreeding can reduce fertility, health and productivity of dairy cattle. The objective of this study was to estimate the inbreeding coefficient of the population of registered Argentine Holstein dairy cattle with genealogical records from the Argentine Holstein Breeders Association database. The population comprised animals with known ancestors, from Argentine origin, and born between 1990 and 2009 corresponding to the genealogy of females from Offspring Registration (grade) and Pedigree Registration listed in the National Official Milk Control System with genetic values for the characteristics milk kg, fat kg, protein kg. Inbreeding coefficients were obtained by implementing a modified recursive algorithm which considers the consanguinity of unknown parents. The average inbreeding for the animals was 3.38%. The trend of inbreeding coef cient by year of birth of the animals for the entire population was 0.13%. When analyzing the average inbreeding according to type of animal registration, it was observed that the value for the females from Pedigree Registry (n = 22174) was 4%, and 3.3% the estimated for the females from the Offsprings Registry. With regard to males (n= 6150, Pedigree Registry) the estimated average inbreeding coefficient was 3.9%. The average inbreeding for the Argentine Holstein female population was lower than that observed in Holstein populations from countries with a dairy activity of relevance. However, due to the positive trend it is suggested to consider strategies to control its growth and maintain genetic variability in the traits of economic importance. Keywords: inbreeding; dairy cattle; genealogy. INTRODUCTION Traditional breeding programs implemented in dairy cattle in the last 50 years have allowed important progress, especially for productive traits. Breeding test implementation, national and international genetic evaluations, and continuous improvements in methods and models have been key to decision making in breeder selection, leading to a sustained increase in the genetic level from one generation to the next. Modern genetic selection programs identify families of animals with greater genetic potential, and using reproductive technologies these genotypes may be distributed in the population. The goals of rearing dairy cattle are generally similar worldwide, but environmental and management conditions may be different, which leads to slightly different selection pressures on a particular trait. In the process of genetic selection, some of the best animals are genetically related as they come from the same families of bulls, thus reducing the genetic variability of the population and giving rise to consanguineous individuals (Neira, 1985). According to Falconer and Mackay (1996) inbreeding depression, as a reduction in the yield of phenotypic means associated with inbred animals, can cause significant economic losses for dairy farmers (Smith et al., 1998; Croquet et al., 2006) and has been associated with reductions in 1 Facultad de Ciencias Veterinarias. Universidad Nacional del Centro de la Provincia de Buenos Aires Paraje Arroyo Seco s/n Tandil, CP 7000, Buenos Aires, Argentina. Correo electrónico: candere@vet.unicen.edu.ar 2 Facultad 2 INIA Las Brujas Ruta 48 Km 10 - Canelones, Rincón del Colorado, Uruguay. Received April // Accepted December // Published online April Inbreeding analysis of the population of Holstein cattle registered in the Official Milk Control System of Argentina

2 April 2017, Argentina 5 milk and fat production, as well as with increases in mortality rates. Therefore, breeding programs should take into account levels of inbred. There is a general consensus that inbreeding adversely affects milk production (Hermas et al., 1987; Miglior et al., 1995; Falconer and Mackay, 1996; Smith et al., 1998; Weigel, 2006), fertility (Smith et al., 1998; Thompson et al., 2000a) and survival (Smith et al, 1998; Thompson et al., 2000a; Sewalem et al., 2006). In Holstein the effects on milk production ranged from -47 kg (inbreeding between 6.25% and 12.5%) to -161 kg (inbreeding between 12.5% and 25%) in lactation at 305 days (Mc Parland et al., 2007). Thompson et al. (2000b) evaluated the effects of inbreeding in Holstein cows, reporting production losses of 35 kg of milk per lactation when inbreeding was 1%, and of 55 kg when inbreeding ranged between 7 and 10%. Fat and protein production losses were proportional to losses in milk production. Wiggans et al. (1995) indicated that the inbred depression was similar for the production traits in the different dairy breeds in the United States, where for the Holstein breed they noted a reduction of 29.6 kg of milk, 1.08 kg of fat and 0.97 kg kg of protein per lactation per each percent point of increase of inbred. Mc Parland et al. (2007) reported an increase rate of 0.10%, between 1994 and 2004, of annual inbreeding increase in Irish Holstein herds. Cassell et al. (2003) studied the importance of having complete genealogies to estimate consanguinity, who compared the inbreeding coefficient using a complete genealogy with a method that uses averages of kinship ratios for missing ancestors (grade) in Holstein populations. With more information, inbreeding and its standard deviation increased from 0.04 ± 0.84 to 1.65 ± 2.05 and 2.06 ± 2.22 for Holstein grade with <31%, 31 to 70%, and 71 to 100% of complete genealogies of five generations. The method using the average of missing ancestors was 2.75 ± 1.06, 3.10 ± 2.21 and 2.89 ± 2.37 for the same groups. Pedigrees of grade animals are often incomplete and may produce erroneous estimates of inbreeding depression that would not be solved by the average insertion of kinship ratios for missing ancestors. Van Doormaal (2008) indicated that the estimated inbreeding values are based on how complete the genealogical information used in their calculation is and that these can not be controlled if the genealogies are incomplete or if they are not accurate. The calculated inbreeding coefficients may underestimate it if genealogical data is poor or deficient, whereas with accurate genealogical inbreeding information quality can be controlled by the use of computer programs that accompany the selection process (Weigel, 2006). Thus, Weigel (2001) (cited by Caraviello, 2004) noted in a study on Holstein breed in the US that average inbreeding in commercial dairy herds was 4.9% (5.1% in random matings and 3.3% using computer programs specially designed to control consanguinity using mating with minimum kinship) and considers that the lack of genealogical information is a limitation to avoid consanguinity. The recent development of molecular technologies and genome studies have enabled the calculation of individual inbreeding coefficients from molecular data. Among the many proposed methods, a very simple and straightforward method seems to be the runs of homozygosity (ROH), homozygous loci of continuous length corresponding to the transmission of haplotypes from parents to offspring. On the one hand, a study by Pryce et al. (2014) shows that different technologies allow estimating inbreeding of genealogies from incomplete genealogies. By comparing the genome effect and the specific location of homozygous sections (ROH) for fertility and milk production traits in 8,853 Holstein and 4,138 Jersey cows, a 1% increase in inbreeding was detected based on both pedigree and genomic data, associated with a decrease in milk, fat and protein production from 0.4 to 0.6% of the phenotypic mean, and an increase in the interval between calving from 0.02 to 0.05% of the phenotypic mean. The optimal contribution is another method for controlling inbreeding. It was studied by Weigel and Lin (2002), Meuwissen (1997), Grundy et al. (1998), Meuwissen and Sonesson (1998), Grundy et al. (2000) and Sonesson et al. (2000). The mean genetic merit is maximized subject to restrictions on the average kinship of the group. On the other hand, Weigel and Lin (2002) reported that long-term control also depends on the correct selection of young bulls entering the progeny tests. The progeny of young bulls have consistently a higher level of inbreeding than that of older bulls (Abdallah and McDaniel, 2002). The difference in age of bulls will certainly be reflected in genetic merit, thus favoring the selection of young bulls, with the risk of increasing consanguinity in the population. Anyhow, the best way to control the level of consanguinity is through its knowledge in the study population, balancing the benefits of genetic progress with the undesirable effects of inbred depression, both short-term and long-term. Consequently, the aim of this work was to estimate the inbreeding coefficients of the population of Holstein dairy cattle registered in the database of the Association of Holstein Breeders, corresponding to the genealogy of females with genetic values of production. MATERIALS AND METHODS The analyzed information was obtained from the Association of Holstein Breeders, which integrates production and breeding information of the National Official Milk Control System, information on morphology of the Morphological Qualifications Program, and information on genealogy from the Breeding Registry (grade) and Pedigree Registry of the breed.

3 ARTICLES RIA / Vol. 43 / N.º 1 According to the distribution of frequencies of animals with known genealogy, we used animals born between 1990 and 2009, Argentine origin, with genetic values for the traits of kg of milk, kg of fat and kg of protein. A total of 422,563 animals (22,174 females from the Pedigree Registry, 394,239 females from the Offspring Registry and 6,150 males) were included. In order to determine the inbreeding coefficient of the animals we used the program INBUPGF90 (Aguilar and Misztal, 2006), which calculates the inbreeding coefficients using a recursive algorithm, assuming non-zero inbreeding for unknown parents, as presented by Aguilar and Misztal (2008). To evaluate the behavior of inbreeding levels as a function of the years we performed a regression analysis, estimating the parameters. The comparisons between slopes were based on the estimation of the 95% confidence interval. For the analysis we used the procedure PROC REG de SAS v9.3 (SAS, Institute Inc, Cary, NC, USA). RESULTS The average inbreeding of the analyzed population (422,563 animals) was 3.38%. Table 1 shows the distribution of the animals according to the percentage of consanguinity. A high percentage of the population (95.39%) had an inbreeding value below 6.25%. 12.8% of the males presented inbreeding values higher than 6.25% while in females it was only 4.4%. Figure 1 shows the behavior of the mean values of inbreeding according to the year of birth for the total studied population and the different groups are part of it. In females and males of the Pedigree Registry, inbreeding levels were slightly higher (with overall averages of 4% and 3.9%, respectively) than the total population (3.4%), and with a greater slope (b= and , respectively). Considering the 95% confidence intervals (Table 2), the slopes in the pedigree animals differ from the females in the Offspring Registry, indicating that the rate of increase of inbred is higher in pedigree animals than in cows of the general rodeo (RC). DISCUSSION It is known that in races with small populations one of the most important problems is the increase of inbreeding coefficient, associated with a reduction in genetic diversity and with inbreeding depression. Inbreeding can not be controlled if accurate and complete records of animals are not available. With an accurate identification of the animal, a mating program may offer the solution to properly attain the accepted inbreeding levels. In Argentina, inbreeding values for dairy cattle have not been reported. However, results were published for beef cattle. Cantet (2008) quantified the level of inbreeding of the parents of 48 Brangus bulls born between 1971 and 1998, 36 born in Argentina and 12 in the USA. The results showed that only one Argentine bull presented a consanguinity of 6.25%, while the remaining 35 were not blood relatives. The averages and inbreeding increases observed in the distribution and trend analyses of this study were similar to those published by different authors for other bovine populations. Ruíz Flores et al. (2006) reported an annual trend of inbreeding in the European Swiss breed of 0.06% between 1983 and 2002, lower than that reported in this study, of 0.134% per year for the entire population. For the Holstein breed in the United States, Hansen (2000) observed an inbreeding increase from 2.7% in 1970 to 6.8% in In view of the increase of inbreeding in Holstein in the United States - from 1.1% to 4.2% between 1970 and some authors warned of the need to reduce the level of kinship of the used bulls (Thompson et al., 2000b). In this study we observed an increase in the average inbreeding for 1990 and 2009 of 2.19% and 4.66%, respectively. Information concerning Danish dairy cattle for 2003 indicated average inbreeding values of 3.9%, 3.4%, and 1.4% for Holstein, Jersey and Danish Red, respectively. The results of this study highlight the need for control of inbreeding in the future (Sorensen et al., 2005). Inbreeding values in the population of Argentine Holstein, lower than those reported by other countries for 2007 (ma- Total population Females Males Inbreeding (%) Frequency % Frequency % Frequency % ³ Total Table 1. Frequency of animals according to the inbreeding percentage for the population. Inbreeding analysis of the population of Holstein cattle registered in the Official Milk Control System of Argentina

4 April 2017, Argentina Inbreeding coefficient Año Total population Females - Pedrigree Females - Offspring registry Males Figure 1. Average inbreeding in the different years for the different groups of animals of the population. Groups of animals b e.e. LI95% LS95% R 2 Total population Females - Offspring registry Females - Pedrigree Males - Pedrigree Table 2. Estimated slope (b) of the inbreeding coefficient as a function of the years for the different groups of animals of the population with production genetic values. les: 5.64%) and 2009 (total population: 4.66%, female Pedigree Registration: 5.63%, females of the Offspring Registration: 4.63%), can be due to the great diversity of genetic material that is imported to the country, as approximately 56% of the semen comes from the US, 30% from Argentina, 13% from Canada and the remaining 1% from countries such as New Zealand and Holland (Casanova et al., 2004). In the last years Germany, Great Britain, Italy and Spain were also incorporated (Technical area of the Association of Holstein Breeders). Finally, it may also be due to the lack of implementation of selection programs. Later, Van Doormaal (2016) indicated that the average inbreeding levels for 2015 in the dairy breeds of Canada were different: 6.22% for Ayrshire, 7.10% for for Holstein and 6.26% for Jersey. Miglior and Burnside (1995) observed between 1976 and 1990 in the Holstein population of Canada that over 90% of the studied animals presented an inbreeding rate below 6.25%. In a study (2001) conducted in Chile, 157 registered pedigree cows from an Overo Colorado dairy herd were analyzed. Results concluded that only 15.3% presented some level of inbred above the levels accepted by the international bibliography (Mujica et al. al., 2012). In Brazil, an inbreeding coefficient of 2.82% was estimated for Gyr dairy cattle, which included lactations from 1960 to 2004 (Filho et al., 2015). In the United States Thompson et al. (2000b) estimated that more than 92% of the cows presented a level of inbreeding below 6%, while for Argentina this study showed that more than 95% did not reach that percentage. In the study by Thompson et al. (2000b) the 6% level was used for comparisons, because in general a level of inbreeding of 6.25% is the result of the mating of a grandparent and granddaughter, and many selection programs through artificial insemination are restricted to this level of inbreeding.

5 ARTICLES RIA / Vol. 43 / N.º 1 Similarly, Hansen (2006) indicated that values should be below the critical figure of 6.25% of consanguinity. It is well known that runs of homozygosity (ROH) have recently been introduced for the analysis of inbreeding in several countries, and although this approach is more reliable than the calculation from pedigree data, the lack of universal norms for the definition and identification of ROH introduces a serious bias that must be considered. The next step would be to investigate the inclusion of this method to supplement future estimates for the national population. CONCLUSION From the obtained results we can conclude that pedigree animals have an annual trend higher than the animals from the Offspring Registry. This difference is in average of a percentage unit. The current average inbreeding of the Argentine Holstein population (3.38%) is lower than that observed in Holstein populations of other countries with relevant dairy production. However, due to its positive trend, it is suggested to consider strategies to control its increase and thus maintain an adequate genetic variation in the traits of economic importance. BIBLIOGRAPHY ABDALLAH, J.M.; MCDANIEL, B.T Proven and young Holstein bulls compared for daughter yields, productive life, somatic cell score, and inbreeding. J. Dairy Sci 85, AGUILAR, I.; MISZTAL, I INBUPGF90. Instituto Nacional de Investigación Agropecuaria, Uruguay. University of Georgia, US. AGUILAR, I.; MISZTAL, I Technical Note: Recursive Algorithm for Inbreeding Coefficients Assuming Nonzero Inbreeding of Unknown Parents. American Dairy Science Association. J. Dairy Sci 91, CANTET, R.J.C Consanguinidad y relación media de parentesco en los padres de toros Brangus. 31. Congreso Argentino de Producción Animal. 15 al 17 de octubre de Revista Argentina de Producción Animal, 28: 1, CARAVIELLO, D.Z Inbreeding in dairy cattle. The Babcock Institute, 1-8. CASANOVA, D.; ANDERE, C.I.; RODRÍGUEZ, E.M.; BER- GONZELLI, P Argentine Genetic Evaluation. Results of Bull Performance. Performance Recording of Animals: State of the Art Proceedings of the 34 th Annual ICAR Conference. Tunez. pp ( CASSELL, B.G.; ADAMEC, V.; PEARSON, R.E Effect of incomplete pedigrees on estimates of inbreeding and inbreeding depression for days to first service and summit milk yield in Holsteins and Jerseys. J. Dairy Sci 86, CROQUET, C.; MAYERES, P.; GILLON, A.; VANDERICK, S.; GENGLER, N Inbreeding depression for global and partial economic indexes, production, type, and functional traits. J. Dairy Sci 89, FALCONER, D.S.; MACKAY, T.F.C An introduction to quantitative genetics. 4.ª ed. Longman Pub. Londres, Reino Unido, p GRUNDY, B.; VILLANUEVA, B.; WOOLLIAMS, J.A Dynamic selection procedures for constrained inbreeding and their consequences for pedigree development.genet. Res. Cambridge. 72, GRUNDY, B.; VILLANUEVA, B.; WOOLLIAMS, J.A Dynamic selection for maximizing response with constrained inbreeding in schemes with overlapping generations. Anim. Sci 70, HANSEN, L.B Consequences of selection for milk yield from a geneticist s viewpoint. J. Dairy Sci 83, HANSEN, L.B Monitoring the Worldwide Genetic Supply for Dairy Cattle with Emphasis on Managing Crossbreeding and Inbreeding. En: Proceeding of the 8 th World Congress on Genetics Applied to Livestock Production, Belo Horizonte (CD-ROM). HERMAS, S.A.; YOUNG, C.W.; RUST, J.W Effects of mild inbreeding on productive and reproductive performance of Guernsey cattle. J. Dairy Sci., 70, 712. MC PARLAND, S.; KEARNEY, J.F.; RATH, M.; BERRY, D.P Inbreeding trends and pedigree analysis of Irish dairy and beef cattle populations. J. Anim. Sci 85, MEUWISSEN, T.H.E Maximizing the response of selection with a predefined rate of inbreeding. J. Anim. Sci 75, MEUWISSEN, T.H.E.; SONESSON, A.K Maximizing the response of selection with a predefined rate of inbreeding: overlapping generations. J. Anim. Sci 76, MIGLIOR, F.; BURSIDE, E Inbreeding of Canadian Holstein cattle. J. Dairy Sci., 78, MIGLIOR, F.; BURSIDE, E.; DEKKERS, J Nonadditive for somatic genetic effects and inbreeding depression cell counts of Holstein cattle. J. Dairy Sci 78, MUJICA, F.; LATRILLE, L.; VERGARA, C Estimación de la consanguinidad en un rebaño lechero doble propósito y su relación con rendimientos productivos y reproductivos: un estudio de caso en el Sur de Chile. Agro sur 40:1, 1-7. NEIRA, R Introducción al estudio de la consanguinidad en animales. Serie publicación docente N.º 11. Santiago, Chile, p PRYCE, J.E.; HAILE-MARIAM, M.; GODDARD, M.E.; HAYES, B.J Identification of genomic regions associated with inbreeding depression in Holstein and Jersey dairy cattle. Genetics Selection Evolution, 46:71. (Disponible: content/46/1/71 verificado 08 de marzo de 2016). REIS FILHO, J.C.; VERNEQUE, R.S.; TORRES, R.A.; LOPES, P.S.; RAIDAN, F.S.S.; TORAL, F.L.B Inbreeding on productive and reproductive traits of dairy Gyr cattle. Revista Brasileira de Zootecnia, 44:5, ( RUÍZ FLORES, A.; NÚÑEZ DOMÍNGUEZ, R.; RAMÍREZ VAL- VERDE, R.; DOMÍNGUEZ VIVEROS, J.; MENDOZA DOMÍN- GUEZ, M.; MARTÍNEZ CUEVAS, E Niveles y efectos de la consanguinidad en variables de crecimiento y reproductivas en bovinos tropicarne y suizo europeo. Agrociencia 40, SEWALEM, A.; KISTEMAKER, G.J. MIGLIOR, F.; VAN DOOR- MAAL, B.J Analysis of inbreeding and its relationship with functional longevity in Canadian dairy cattle. J. Dairy Sci 89, SMITH, L.; CASSELL, B.; PEARSON, R The effects of inbreeding on the lifetime performance of dairy cattle. J. Dairy Sci 81, SONESSON, A.K.; GRUNDY, B.; WOOLLIAMS, J.A.; MEUWIS- SEN, T.H.E Selection with control of inbreeding in populations with overlapping generations: A comparison of methods. Anim. Sci 70, 1-8. SORENSEN, A.; SORENSEN, M.; BERG, P Inbreeding in Danish dairy cattle breeds. J. Dairy Sci 88, THOMPSON, J.R.; EVERET, R.W.; HAMMERSCHMIDT, N.L. 2000b. Effects of inbreeding on production and survival in Holsteins. J. Dairy Sci 83, Inbreeding analysis of the population of Holstein cattle registered in the Official Milk Control System of Argentina

6 April 2017, Argentina 9 THOMPSON, J.R.; EVERETT, R.W.; WOLFE, C.W. 2000a. Effects of inbreeding on production and survival in Jerseys. J. Dairy Sci 83, VAN DOORMAAL, B Demystifying inbreeding. Canadian Dairy Network. (Disponible: php?id=143 verificado 08 de marzo de 2016). VAN DOORMAAL, B Inbreeding Update. Canadian Dairy Network. (Disponible: verificado 10 de agosto de 2016). WEIGEL, K.A Controlling inbreeding in modern breeding programs. J Dairy Sci 84, 177-E184. WEIGEL, K.A Controlling Inbreeding in Modern Dairy Breeding Programs. WCDS Advances in Dairy Technology 18, WEIGEL, K.A.; LIN, S.W Controlling inbreeding by constraining the average relationship between parents of young bulls entering AI progeny test programs J. Dairy Sci 85, WIGGANS, G.; VANRADEN, P.; ZUURBIER, J Calculation and use of inbreeding coefficients for genetic evaluation of United States dairy cattle. J. Dairy Sci 78,