ARTÍCULOS ORIGINALES

Genealogical and molecular analysis of an Argentinean Angus seedstock herd

Análisis genealógico y molecular de un plantel Angus de Argentina

 

Corva P.M.^1*, Colavita M.I.¹, Legaz G.², Martínez M.²

¹ Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Unidad Integrada Balcarce. C.C. 276, 7620 Balcarce, Argentina
² Laboratorio de Genética Aplicada, Sociedad Rural Argentina. Juncal 4431, 2º Piso, 1425 Buenos Aires, Argentina.
* Author for correspondence corva.pablo@inta.gob.ar

Fecha de recepción: 11/05/2015
Fecha de aceptación de versión final: 18/08/2015

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ABSTRACT

Introduced in Argentina from the British Isles in 1879, the Angus progressively became the most popular beef cattle breed in the country. In this article the analysis of genealogical and molecular information generated in the registration process of progenies from an Angus seedstock herd is presented. The objectives were to analyze the genetic structure of the herd, and to use the acquired information to get insight of the history of the Angus breed in Argentina. Pedigree information from 16,611 individuals born between 1954 and 2012 was analyzed, including Black and Red Angus. Also available were genotypes of 17 microsatellites from 470 individuals born between 2005 and 2012. Identification of the most influential ancestors showed a trend that is consistent with the evolution of selection objectives, mostly associated with changes in body size. Generation intervals in the male pathways also reflected drastic changes in selection objectives over time. Molecular kinship and genealogical average relatedness have been steadily increasing. Molecular FIS was -0.023, indicating that matings were planned in order to avoid inbreeding, which increased 0.70% per Equivalent Generation. Genetic distance showed that Black and Red Angus are two separated lines within this herd. Molecular and genealogical information jointly allowed for a reliable characterization of the genetic structure of the herd, a strategy that should be extended to the entire breed to monitor genetic variability and to help in breeding decisions.

Key words: Population structure; Coancestry; Microsatellites; Inbreeding.

RESUMEN

La raza Angus fue introducida en Argentina desde las Islas Británicas en 1879 y progresivamente se convirtió en la principal raza para carne del país. En este trabajo se analiza información genealógica y molecular generada en el proceso de inscripción de reproductores de un plantel Angus Puro de Pedigree, con dos objetivos: analizar la estructura genética del plantel y en función de la misma, revelar aspectos relevantes de la historia de la raza en el país. Se utilizaron registros genealógicos de 16.611 animales (Negros y Colorados) nacidos entre 1954 y 2012 y los genotipos de 17 microsatélites en 470 animales nacidos entre 2005 y 2012. La identificación de ancestros más influyentes y la estimación de intervalos generacionales mostraron una tendencia consistente con la evolución de los objetivos de selección asociados a cambios en el tamaño a través del tiempo. La coancestría molecular y el parentesco están aumentando en forma sostenida, pero el incremento en consanguinidad fue sólo 0.70% por generación equivalente. El FIS molecular igual a -0.023 indica que los apareamientos se planean para minimizar la consanguinidad. Las distancias genéticas entre Angus Negro y Colorado muestran que ambos se manejan como líneas separadas. La utilización de información genealógica y molecular permitió la caracterización de la estructura genética del plantel, y esta estrategia debería extenderse a toda la raza para monitorear el incremento de la consanguinidad y la pérdida de variabilidad y ayudar en las decisiones de selección.

Palabras clave: Estructura poblacional; Coancestría; Microsatélites; Consanguinidad.

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INTRODUCTION

Introduced in Argentina from the British Isles in 1879, the Angus breed was very successful and progressively became the most popular beef cattle breed in the country. Currently, approximately 50% of the stock corresponds to pure-blood Angus and another 20% to crosses (Argentinean Angus Association, 2014). In this process, Angus breeders had to adapt to several changes in selection objectives, to the point of having to reverse the path taken, as it was the case of the selection for higher growth rate and body size that dominated selection objectives in the 1970s-1980s and which led to the production of extremely large animals that performed poorly in extensive production systems (Molinuevo, 2005). Since then, breeders have been successfully working on the definition of a local biotype, adapted to the prevailing production systems and markets. The process of registration of all cattle breeds in the Argentinean Herd Book requires paternity confirmation (Sociedad Rural Argentina, 2014). Parentage verification was originally based on blood groups analysis, but this system was replaced by the use of molecular markers in 2005. Since then, more than 135.000 animals of different breeds have been genotyped and these procedures have contributed to the creation of an extensive database of genomic information that it is not used for other than administrative purposes. Conversely, genealogical information generated by the registration process is more valued by breeders because it is a key resource for genetic evaluation programs (estimation of Breeding Values). However, other applications of this information are still underappreciated (for example, monitoring trends in inbreeding and genetic variability).
The purpose of this work was therefore twofold: to analyze the genetic structure of a traditional Angus seedstock herd, taking advantage of two sources of information (genealogical and molecular) that are available with no additional costs but which are currently not fully appreciated, and secondly to use these results to obtain insight of the history of the Angus breed in Argentina.

MATERIAL AND METHODS

Genealogical information
The pedigree information from the Angus Herd Book was provided by the Argentinean Rural Society (“Sociedad Rural Argentina”, SRA) with consent of the herd owner. Unlike other countries, in Argentina the Angus Association considers the Black and Red Angus as two varieties of a single breed, and both were included in the files. Information was checked for consistency with the program Pedigree Viewer (Kinghorn and Kinghorn, 2014). Inconsistent information corresponding to sex, birth dates, or paternity were confirmed at the SRA web browser (http://www.sra.org.ar/rrgg/) and manually edited. Animals with pending registration but with genotype information (see below) were manually added to the pedigree files. The final pedigree included 16,611 animals born between 1954 and 2012.

Genealogical analyses
For each individual, the number of fully traced generations (those with 2g ancestors known, where g is the number of generations back), the maximum number of generations traced (from the individual to the furthest ancestor) and the equivalent complete generations (computed as the sum of ½n over all known ancestors, where n is the number of generations separating the individual and the known ancestor) were computed. Genealogical information was analyzed to obtain the full coancestry matrix (Malècot, 1948), the individual coefficient of inbreeding (F) (Wright, 1969) and the average relatedness coefficient (AR) (Goyache et al., 2003). The AR was defined as the probability that an allele randomly chosen from the whole population belonged to a given animal. The AR of an individual can be computed as the average of the coefficients in the row corresponding to the individual in the numerator relationship matrix (Gutierrez et al., 2003). The AR is twice the average genealogical coancestry. The coefficient of coancestry (fij) between individuals i and j is defined as the probability that at a neutral, autosomal locus an allele drawn randomly from individual i is identical by descent (IBD) to an allele drawn randomly from individual j. The inbreeding coefficient of an individual i (Fi), is defined as the probability that the two alleles carried by this individual at a given locus are IBD. Effective population size and increase in inbreeding (ÄF) were estimated by computing the regression of the individual inbreeding coefficient over the number of equivalent generations, where the regression coefficient b is the increase in inbreeding between two generations and Ne = 1/2b (Gutierrez and Goyache, 2005). The genetic contribution of ancestors to the herd was estimated according to Boichard et al. (1997). Generation intervals were defined as the average age of parents at the birth of their progeny kept for reproduction. They were calculated for the four pathways of selection: sires to produce sires (SS), dams to produce sires (DS), sires to produce dams (SD) and dams to produce dams (DD) (Marquez and Garrick, 2007). All the pedigree analyses were conducted using the Endog v4.8 program (Gutierrez and Goyache, 2005).

Molecular analyses
The Laboratory of Applied Genetics of SRA provided all the genotypes corresponding to animals from the herd that were available by the end of 2012, alongside of an independent sample of 200 Angus individuals to be used as a reference of the breed. Total DNA was isolated from tail hair and semen samples following standard procedures. A set of 12 STR markers from the International Society of Animal Genetics (ISAG) core panel and 5 additional microsatellites were analyzed: BM2113, BM1824, INRA23, BM1818, TGLA227, TGLA126, ETH225, CYP21, SPS115, TGLA122, ETH10, BRR, ETH3, TGLA53, BMS510, BL1043 and RME40. The PCR fragments were separated by electrophoresis in a 3730 XL ABI Sequencer (Applied Biosystems). Alleles size were scored against GeneScan™ 500 LIZ® Size Standard (Applied Biosystems) using the Data Collection v3.0 software (Applied Biosystems). Pedigree information and birth dates were checked and a file with the molecular information of 470 animals born between 2005 and 2012 was created. Because this group had both genealogical and molecular information, it was used as a reference population when needed. Basic descriptive parameters of population genetics: Number of alleles per marker (Na), effective number of alleles (Ne), observed (Ho) and expected heterozygosity (He), significance of Hardy Weinberg Equilibrium departures (HWE), polymorphic informative content (PIC) and Fixation index (F) were estimated with the Genalex 6.5 software (Peakall and Smouse, 2006). The PIC refers to the value of a marker for detecting polymorphism within a population (Botstein et al., 1980). It was computed

where pi and pj are the frequency of alleles i and j of a given locus. Observed heterozygosity was estimated as Ho = (No. of Heterozygotes /N) and expected heterozygosity was estimated as He = 1 - Ópi 2 where pi is the frequency of the ith allele for the population and Ópi 2 is the sum of the squared population allele frequencies. The Fixation index, which is equivalent to FIS of Wright (1969), was computed as F = 1 - (Ho / He). Other analyses corresponding to molecular information were conducted using the Molkin v3.0 program (Gutierrez et al., 2005). The molecular coancestry matrix among genotyped individuals was computed. The molecular coancestry (or kinship), fMij between individuals i and j at a given locus is the probability that two alleles at the locus taken at random from each individual are equal (identical by state, IBS): fMij, L = ¼ [I11 + I12 + I21 + I22]. Ixy is 1 when allele x on locus L in individual i and allele y in the same locus in individual j are equal, and zero otherwise. Molecular coancestry between two individuals was obtained by averaging fMij, L over L analyzed loci. Molecular mean kinship (Mk) was computed as the average molecular coancestry of each individual with the rest of the population. The molecular coancestry of an individual i with itself is the self coancestry (si) which is related to the coefficient of inbreeding of the individual (Fi) by the expression Fi = (2 si) – 1 (Toro et al., 2011). For individual pairwise comparisons the proportion of shared alleles was estimated as PSAij = Óu S/ 2u, where the number of shared alleles S is summed over all loci u. Distance between individuals i and j was estimated by DSAij = 1 - PSAij (Chakraborty y Jin, 1993). Based on the DSA matrix, an unrooted Neighbor Joining tree was constructed using the program Mega 6.0 (Tamura et al., 2013).

RESULTS

The genealogy of the whole population (16,611 records) spanned 14 maximum generations. There were 283 sires and 4,596 dams, with maximum paternal and maternal family sizes of 1,673 and 39 individuals, respectively. Because we got access only to the records corresponding to the herd under study some information was missing, especially that corresponding to sires that were not bred within the herd. These result affected the completeness of pedigree information, as it can be seen in Figure 1.

Figure 1. Completeness of pedigree information going back three generations in the analyzed Argentinean Angus seedstock herd. PGS = paternal grandsires; PGD = paternal granddams; MGS = maternal grandsires; MGD = maternal granddams; PGSS = sires of paternal grandsires; PGSD = dams of paternal grandsires; PGDS = sires of paternal granddams; PGDD = dams of paternal granddams; MGSS = sires of maternal grandsires; MGSD = dams of maternal grandsires; MGDS = sires of maternal granddams; MGDD = dams of maternal granddams.

Generation intervals and most influential ancestors
The estimated generation intervals (Table 1) were within the range of values recorded for other cattle populations (Gutierrez et al., 2003; Marquez and Garrick, 2007; Santana Jr. et al., 2012) with the exception of the Sire- Son pathway, the most relevant in terms of genetic progress, which was surprisingly long when compared to the other three pathways. It can be seen that among the most influential ancestors there are bulls from the 1960´s (Table 2). Moreover, one of these comparatively older bulls, “Ankonian Big Bandoliermere 10”, made the largest contribution to the genetic pool also between 2005 and 2012. This seemingly inefficient selection strategy can be understood if the changes that occurred in the selection objectives over time are taken into account, as it will be discussed later. Also related to the successive changes in selection objectives, the comparison of influential ancestors between the population as a whole and the reference group showed a trend towards a higher influence of bulls bred in local herds (Table 2). There were six local sires out of fourteen in the first case, and four out of six in the second case (bulls such as “Tres Marias 5887 Hornero-T/E-“ and “Moon 16621 Ritmo”).

Table 1. Generation intervals computed in four pathways of selection in an Argentinean Angus seedstock herd.

Table 2. Ancestors explaining 50% of the genetic variability in the whole dataset and in the group of genotyped animals of the analyzed Argentinean Angus seedstock herd.

Inbreeding Only
86 matings between half sibs and 148 matings between parents and offspring were detected and there were only 640 individuals with F ¡Ý 1% when the whole dataset was considered. When the analysis was restricted to the last three generations to have a better estimation of recent inbreeding, 448 individuals with F ¡Ý 3% were found. The average F in each case was 0.41% and 0.38%, respectively. The increase in inbreeding (ÄF) per equivalent generation was 0.70% (Ne = 71).

Molecular information

Descriptive statistics of the microsatellite panel are shown in Table 3. Allele frequencies corresponding to the herd under study were compared to those of an independent sample of 200 Angus individuals, and there were no major discrepancies between the two groups (data not shown). Only six markers out of seventeen deviated from HW equilibrium. Most markers tended to have negative coefficients of fixation, which is indicative of an excess of heterozygotes. Mean molecular coancestry and molecular FIS were 0.33 and -0.023, respectively. Inbreeding estimated from marker information (Identity by State, IBS) was 0.29. Figure 2 shows that both average molecular coancestry and AR (twice average genealogical coancestry) significantly increased with respect to equivalent generations (y = 0,27 + 0,015 x; R2 = 0,11 and y = -0,004 + 0,001 x; R2 = 0,21 respectively). The estimation of genetic distances based on markers (Figure 3) showed that almost all Red Angus individuals in the herd were grouped together, indicating that Red and Black Angus are most likely conducted as two separated lines in this herd.

Table 3. Number of genotyped animals (n), number of alleles per marker (Na), effective number of alleles (Ne), observed (Ho) and expected heterozygosity (He), significance of Hardy Weinberg Equilibrium departures (HWE), polymorphic informative content (PIC) and coefficient of fixation (F) for the microsatellite panel used in Argentina for parentage verification in cattle.

Figure 2. Changes in Average Relatedness (circles) and Molecular Mean Kinship (squares) as a function of the number of equivalent generations of 470 genotyped animals from an Argentinean Angus seedstock herd. The arrow indicates a group of 48 animals with comparatively higher AR, all sired by Ankonian Big Bandoliermere 10 (born in 1969).

Figure 3. Unroooted neighbor-joining tree showing genetic distances based on (1 - Proportion of Shared Alleles) of progenies from an Argentinean Angus seedstock herd that were genotyped with a panel of 17 microsatellites. Only two progenies of each of 55 sires are shown. Black circles: Black Angus. Grey circles: Red Angus.

DISCUSSION

The main reason to choose the herd that is described in this paper was its long tradition in breeding Angus cattle and its influence in the evolution of the breed in its early stages in the country. In many breeds, the hierarchical structure of the population and the attempts to avoid inbreeding make many males to be usually bred in herds other than where they were used as parents (Marquez and Garrick, 2007). Most breeders do not produce bulls to breed bulls (SS) in their own herds, and always new genetic lines are evaluated together with the ones already in use. For many years, successive changes in breeding goals were associated with the use of foreign SS (first from the British Isles, then from the U.S.A.) in Argentina. Yet currently there is a higher influence of local genetic lines (Firpo Brenta, 2003). On the contrary, most breeders keep their own replacement females. Due to regulations of the SRA, we only got access to information from this particular herd with previous consent of the owner. That is why there is much more information on the side of the pedigree corresponding to dams, which were mostly bred within the herd (Figure 1) and not because the missing males and females were unknown.
Consideration of the most influential male ancestors in the herd (Table 2) provides a good description of the history of the breed, which in turn reflects the same process in other countries (U.S.A., Canada) (Ritchie, 2002). The original Angus introduced in America was represented by small-framed, early maturing animals (“Old type Angus”). By the late 1960´s, selection of the Angus breed in the U.S.A. moved towards the search of leaner, more efficient, larger-framed cattle, following changes in life style and industry needs (Ritchie, 2002). This process had strong influence on selection trends in Argentina since the mid- 1970´s (Firpo Brenta, 2003). Since then, growth rate and body size prevailed in the selection objective of most breeders, with strong influence of imported germplasm. For example, sons and grandsons of the sire “Blacklock Mc Henry 13 Y” (born 1967) (Table 2) were closely linked to this process in its early stages; one of the sons of “Blacklock Mc Henry 13 Y”, “Verbena 2440 Greatnorterndynamo” was himself an influential sire of the herd. The bull “Primavera Gran Milagro 6970-T/E” (born 1986) (Table 2) that also belongs to that stage in the history of the breed, still appeared in the local Angus Sire Summary in 2010. His EPDs (Expected Progeny Differences) placed him among the top 5%, 2% and 20% of all evaluated sires for Birth Weight, Weaning Weight and Final Weight (18 months), respectively, confirming that he was among the largest and fastest-growing bulls in the local population. Some of the most influential ancestors in this herd have been widely used across the breed, and themselves and/ or their progeny excelled in the internationally renowned “Exposición Rural de Palermo”, the most important livestock show of the country, showing the connection between the herd and the local genetic pool at large (Table 2; Firpo Brenta, 2012). Despite the importance given to objective measurements and genetic evaluation as tools for selection, show ring results strongly influence breeding decisions. The selection towards larger-framed cattle following the trend of other countries got severe criticism, because it underestimated strong genetics x environment interactions (Molinuevo, 2005). Extreme animals did not adapt well to local production systems; especially those based on direct grazing due to their higher nutritional requirements, and also required higher slaughter weights that did not fit the local market. Under these conditions, the genetic flux among tiers in the population was virtually disrupted. Therefore, selection objectives needed to be reformulated again. The change in selection objectives along time also provides an explanation for apparently odd results about generation intervals (Table 1). The longest generation intervals correspond to the most important selection pathway (sire-son). This is because bulls born in the 1960’s matched selection criteria in recent years and the availability of frozen semen allowed the intensive use of them, even in present time. In fact, these bulls were among the most influential ancestors of the herd (Table 2). “Ankonian Big Bandoliermere 10” still appeared in the local Angus Sire Summary 2014. This bull was placed among the top 75%, 90% and, 95% of all evaluated sires for Birth Weight, Weaning Weight and Final Weight (18 months), respectively. During the transition from the Old type to the New type Angus in Argentina, the Frame Score (FS) developed at the University of Missouri (BIF, 1996) was one of the traits with most influence on the breeding goals. For the sake of comparison, the FS of representative Old Type Angus, New Type Angus and current Angus males from local seedstock herds would be around 2, 9 and 6, respectively (Argentinean Angus Association, 2014); the corresponding hip heights for such FS at 18 months of age are 118 cm, 153 cm and 138 cm, respectively. These figures are proof of the dramatic changes along time of what was considered to be the most adequate cattle type. Although the use of comparatively older sires cannot be considered a generalized strategy, genetic trends in this herd match those of the whole breed (Argentinean Angus Association, 2014). Emphasis is now placed on growth rate and muscling, trying to keep birth weight and adult cow size unchanged at the same time (Figure 4). These selection criteria are consistent with the search since the mid-1990’s of what was considered “a local biotype”, which is somewhere in between the “Old type” and “New type” Angus. The bull “Tres Marias 5887 Hornero-T/E-“ (Table 2) which belongs to a highly influential genetic line in present time, is a good example of that new biotype.

Figure 4. Genetic trends of Birth Weight, Live Weight at 18 Months of Age, Rib Eye Area and Hip Height in the Argentinean Angus seedstock herd under study (Adapted from the Angus Genetic Evaluation Program, Argentinean Angus Association, http://www.angus.org.ar/)

Avoiding inbreeding has always been a major concern in populations under selection, because it is associated with the conservation of genetic variability and the prevention of inbreeding depression. According to Figure 2, AR and molecular coancestry are steadily increasing in the herd, demanding close attention to mating design to avoid inbreeding. The increase in molecular coancestry implies a certain degree of genetic erosion (decreasing “effective number of alleles”; Caballero and Toro, 2002). In an ideal situation of random mating without population subdivision, the AR equals one half of F in the next generation. However, the negative FIS estimated in this case implies that the average F does not exceed the between individual coancestry (Royo et al., 2007), confirming that matings were properly managed in what relates to inbreeding avoidance (resulting in an increase of 0.70% per equivalent generation). The clear distinction between Black and Red Angus in the analyses of genetic distance was proof of the usefulness of marker information if genealogical information were scarce: a relatively small set of markers has the power to discriminate genetic lines within a breed (Figure 3). While some local breeders pay little attention to coat color of progenies out of black or red cows, some others keep them as separate lines, as it seems to be the case in this herd. The genetic distance between both varieties is especially noticed when genetic material is imported from countries like the U.S.A. for example, where Black and Red Angus are two separated breeds with marked differences in breeding goals. Two assumptions of the analysis of relatedness based on pedigrees are that all founders are unrelated and not inbred. Even if those assumptions were met, recombination during meiosis still makes IBD probabilities an imprecise estimation of genome sharing: human halfsibs, for example are expected to share half of each parental chromosome, but the actual amount shared ranges from 37% to 63% (Speed and Balding, 2015) and the individual deviation of realized IBD becomes relatively larger for more distant pedigree relationships. Moreover, in the present case inbreeding could have been underestimated to some extent due to pedigree completeness (Figure 1). For these reasons, the estimation of genome sharing directly from molecular marker information is considered a much more relievable option. High-density SNP panels are now available and the analysis of runs of homozygosity (ROH) based on SNP genotypes have been proposed as a good indicator of individual autozygosity and potentially inbreeding depression (Purfield et al., 2012; Speed and Balding, 2015). However, few animals have been genotyped with that kind of panels in Argentina, while the information on microsatellites is already available at no additional cost. Therefore we considered worthwhile to evaluate the potential applications of this source of genomic information.
To our knowledge, this is one of the first analyses that take advantage of the SRA genealogical and molecular databases to analyze genetic structure in a local herd in the way that is presented here. One strong assumption when using marker information for the estimation of relatedness is that allele frequencies from the founder population remains unchanged (Toro et al., 2011) whereas they are most likely modified by drift and selection. In fact, there is evidence that genomic regions harboring microsatellites are under selection in beef cattle, one example being marker ETH10 (DeAtley et al. 2011). Therefore, this molecular information should be interpreted under the premise that F estimated with microsatellites largely relies on IBS and probably overestimates relatedness. Even if this were the case, in a situation of missing genealogical information, molecular information could be an aid to get an approximate estimation of kinship (Figure 2) and genetic distances (Figure 3) and also to design mating schemes that minimize inbreeding. The estimation of inbreeding depression (Leroy, 2014) based on either genealogical or molecular data and using the phenotypic records from the Angus Genetic Evaluation Program could also give an appraisal of the usefulness of each source of information. In this paper we have used useful genealogical and molecular information generated in the registration process to characterize the genetic structure of a herd that has been closely involved and has contributed to define the main features of the evolution of the Angus breed in Argentina. Cattlemen are not fully aware of the availability and potential applications of these resources, which can be deployed together with the better known genetic evaluation for the estimation of Breeding Values (as Expected Progeny Differences). Despite the worldwide wealth of genomic information in cattle, very few animals have been genotyped with high-density SNP panels in Argentina so far, making the microsatellite information a valuable asset. An SNP panel suitable for parentage verification has already been developed and ISAG is endorsing its application to eventually replace the microsatellite panel (ISAG, 2012). Fortunately, experimental strategies have been already implemented to connect both systems (McClure et al., 2012). Independently of the molecular basis of the information, the rationale of the analysis described here will remain unchanged. Moreover, it could be applied to the entire breed.

ACKNOWLEDGMENTS

This work was financially supported by Universidad Nacional de Mar del Plata, Project AGR377/12.

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