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ANIMAL GENETICS |
,2
* Estação Zootécnica Nacional, Fonte Boa, 2005-048 Vale de Santarém, Portugal; and
Faculdade de Medicina Veterinária, Universidade Técnica de Lisboa, 1300 Lisboa, Portugal
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Alentejana • cattle • genetic diversity • inbreeding • population structure
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Management of genetic diversity of a breed is essential for its sustainable use in the future because a limited number of breeders will inevitably lead to increased inbreeding and thus to a reduction in additive genetic variance (Falconer and MacKay, 1996
), and possibly to inbreeding depression (Burrow, 1993). As a consequence, controlling inbreeding is usually one of the major targets in conservation and selection programs (Meuwissen and Woolliams, 1994; Hill, 2000).
Classically, monitoring of genetic diversity has been carried out by assessing the evolution of inbreeding and relationships (Wright, 1922) in the population of interest, often converted to effective population size, which is regarded as a good indicator of the risk of genetic erosion (FAO, 1998). Nevertheless, inbreeding-related parameters are dependent on the completeness of pedigree information, and changes in inbreeding due to different breeding practices (e.g., genetic bottlenecks) are not immediately perceivable. Therefore, parameters based on the probability of genetic origin from different herds (Robertson, 1953), founders (James, 1972; Lacy, 1989), and ancestors (Boichard et al., 1997) have been proposed as complementary indicators because they provide more insight into changes occurring in the population over a short period of time (Boichard et al., 1997).
The objectives of this study were to 1) characterize genetic diversity in the Alentejana breed of cattle based on demographic trends, and 2) investigate the major factors affecting genetic erosion in this breed, to establish conservation strategies aimed at maintaining genetic diversity for the future.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The Alentejana breed is traditionally raised under extensive conditions, in oak- and cork-tree forests, or integrated with grain production systems in dry-lands. In the mid-20th century it was under serious threat of extinction due to uncontrolled and unplanned cross-breeding with exotic breeds, but the census size has increased since then. There are now approximately 11,000 cows registered in the herdbook, which is managed by the breeder’s association. Reproduction takes place essentially by natural mating, with very limited use of artificial insemination, given the difficulties associated with estrous detection in extensive production systems. Producers generally breed their own replacement females, while bulls are either from their own herd or obtained from other herds. From 2003 onwards, a genetic evaluation by BLUP-Animal Model methodology has been in place, applied to reproductive, growth, and carcass traits (Carolino et al., 2006).
Data
The demographic analysis of the Alentejana cattle breed was based on herdbook records obtained from Associação dos Criadores de Bovinos da Raça Alentejana. These records contained information on individual identification number, sex, sire, and dam identification number, birth date, and herd of origin. Records were checked to ensure consistency of the data and edited for duplicate records and compatibility of birth dates and individual identifications. Data analyzed included records on 99,020 animals registered in the herdbook between 1968 and 2004, as well as additional pedigrees of 1,542 ancestors born between 1940 and 1968, for a total of 100,562 animals from 155 herds in the data set.
The baseline information was used to assess the evolution of number of registered animals and herd size, age distribution of sires and dams, and number of offspring per parent.
Pedigree Analysis
The degree of pedigree completeness was evaluated by calculating the equivalent number of complete generations known per animal (ni) as
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where ns and nd are the number of generations known for the sire and dam, respectively, when s and d are known; if s or d are unknown, then ns or nd, respectively, assume a value of –1. Base animals were assigned a number of generations known equal to 0.
The additive genetic relationships among all pairs of animals (aij) and the individual coefficients of inbreeding (Fi) were computed based on the numerator relationship matrix (Van Vleck, 1993) among all animals. The regression coefficient of individual inbreeding on year of birth was obtained, and this was considered to be the rate of inbreeding per year (
F/y).
The mean generation interval was computed as the average age of sires and dams of all calves born, and also for the 4 paths of selection (average age of sires of sires, sires of dams, dams of sires, and dams of dams). The generation intervals for the 4 paths of selection were averaged to obtain a pooled generation interval (L), which was used to compute the rate of inbreeding per generation (F/g) as F/g = L (F/y). The effective population size (Ne) was then calculated as (Falconer and MacKay, 1996):
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The genetic contributions of founder animals, ancestors, and herds were computed, as described by James (1972) and Boichard et al. (1997). Briefly, these methodologies are based on the assumption that an allele taken at random from any locus of an individual has a probability of 0.5 of having been received from a given parent, 0.25 from a grandparent, etc. Applying this probability of gene origin to a pedigree, it is possible to calculate the expected genetic contribution (qk) of the kth founder animal to the gene pool of an individual or group of individuals. For this calculation, an animal with both parents unknown is considered a founder, and the unknown parent of an individual with only 1 parent known is also considered as a founder animal.
When several pedigree generations are considered, a reference population can be defined (e.g., the group of animals born in a given time-period), and the proportional contribution of different founders evaluated, such that the sum of all founder contributions to the population equals 1. Therefore, when evaluating the genetic structure of a population, the total number of founders (f) is of limited usefulness because founder contributions are generally represented in unequal proportions. It is more appealing to consider the effective number of founders, which is defined as the number of equally contributing founders that would be expected to generate a similar amount of genetic diversity in the population studied. The effective number of founders (fe) can then be calculated from the genetic contributions of the f founders as
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If all founders have the same contribution to the population, then fe = f, but in the more frequent situation of unequal founder contributions, then fe < f.
The same principles were used to estimate the contributions of different founder herds to the genetic pool of the reference population, and from those genetic contributions the effective number of founding herds was calculated.
The existence of bottlenecks along the pedigrees was assessed by evaluating the effective number of ancestors (fa), which was estimated as the number of ancestors (founders or not), which, if they all had the same contribution to the reference population, would have resulted in the observed genetic diversity, and calculated as
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In these expressions, pk corresponds to the marginal contribution of the kth ancestor (i.e., its contribution beyond that already explained by its ancestors) to the reference population, qk is the total contribution of the same ancestor, and akj is the relationship between the kth ancestor and each 1 of the n – 1 ancestors already considered.
The number of founder Y chromosomes currently represented was assessed by analyzing the transmission along the sire path from founding bulls to male calves in the reference population. From the proportion of Y chromosomes represented, an effective number of Y founders was calculated, using the same principles defined for fe and fa. Similar procedures were used to evaluate the transmission of mitochondrial DNA (mtDNA) along the dam path, from founding cows to calves in the reference population.
The genetic contribution of different herds to the current genetic pool was evaluated according to Robertson (1953), through the estimation of the effective number of herds supplying sires (Hs), which results from the probability (Cs) of 2 animals taken randomly from the population being the offspring of 2 sires with the same herd of origin. Therefore, Hs corresponds to the number of herds that would account for the observed genetic variability if all herds had the same contribution. The probability Cs of sires belonging to the same herd was estimated as a function of the number of sires originating from the ith herd (si), assuming a total of H herds supplying sires to the current population, as
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The same principles were used to estimate the effective number of herds supplying paternal grandsires and great-grandsires to the reference population, based on the probability of 2 animals having those ancestors born in the same herd.
For the purposes of this study, the reference population was considered to be the group of calves (n = 28,631) registered in the herdbook with birth year between 2000 and 2003. The genetic contributions of founders, ancestors, and herds were evaluated for this group of animals.
All demographic analyses were performed with software specifically developed for this purpose, while statistical analyses were carried out with the GLM procedure (SAS Inst. Inc., Cary, NC).
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RESULTS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Currently, there are nearly 10,700 registered cows and 120 herds enrolled. A steady increase in the number of cows registered annually was observed up until 1998, but the number leveled off after that year. The average herd size is 85.5 ± 63.4 registered cows and 70.9 ± 45.0 calves per herd-year, with nearly 20% of the herds registering less than 20 purebred calves each year.
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. The mean ages for sires and dams at calf’s birth were 6.0 ± 2.3 and 6.8 ± 3.2 yr, respectively, with the first offspring usually produced at 3 yr of age in cows, and somewhat later in bulls. These results indicate that, when compared with cows, the use of bulls started at a later age, but that they were also replaced at a faster rate. Nevertheless, nearly 10% of the offspring were sired by bulls at or above 10 yr of age, whereas the percentage of calves produced by cows of the same age range was about 24%. The resulting generation intervals (Table 1) for calves had a mean of 6.5 yr and were higher for cows than for bulls. Similarly, when generation intervals were evaluated for the 4 paths of selection, they were almost 1 yr longer for the dam paths.
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), with nearly one-half of the bulls siring less than 50 calves registered, whereas about two-thirds of the calves were produced by the 23% of the bulls with more than 150 calves registered.
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, for all calves and for those born in the period of 2000 to 2003. Pedigree filling improved when only the last few years of information are considered, with an overall mean of 86.6% of the great-grandparents known, even though there is still some lack of pedigree information, especially on the dam path. The degree of pedigree completeness was also assessed by the number of generation equivalents, which corresponds to the average number of complete generations known in the pedigree of an individual. The number of generation equivalents increased from nearly 1 for calves born in the 1960s and 1970s to over 4 generations in calves born in 2003 (Figure 5).
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) indicates a steady increase over time, from a mean value of 0.8% for calves born in 1980, to an average of 8.5% in calves born in 2003. Throughout the years, the proportion of noninbred calves dropped steadily (Figure 5), such that only 18% of the calves born in 2003 were not inbred. In the reference population, the mean inbreeding per herd ranged between 0.2 and 28.1%, as shown in Figure 6.
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).
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). Three herds were identified as having the highest relationship with the remaining 99 herds active in the reference population. Overall, these 3 herds had an average relationship with the other herds of 0.051, 0.047, and 0.031, respectively. Very few herds had a null relationship with the 3 most influential herds.
The results of the retrospective evaluation of cumulative genetic contributions of founders, ancestors, and herds to the reference population are summarized in Table 3 and represented in Figure 7. Overall, there were 6,842 founders, of which 671 were sires and 6,171 were dams. The cumulative genetic contributions of the most important founders, ancestors, and herds (Figure 7) show a steep increase in the early stages of the curves, indicating that a small number of animals and herds have a strong influence on the breed. For example, one herd alone accounts for nearly 19% of the current genetic diversity, whereas the most important ancestor contributes about 10% of this diversity. However, the corresponding contribution of the major founder was only 3.5%. Overall, 50% of the genetic pool is accounted for by the contributions of 8 herds, 46 founders, and 33 ancestors, with the 2 most influential ancestors contributing 15.1% (Table 3).
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). The number of herds supplying great-grandsires was approximately one-third of the number supplying sires and less than 10% of the total number of herds. The very unbalanced contribution of ancestors over time resulted in an effective number of ancestors of 55.0, which corresponds to less than half of the effective number of founders. As expected, the vast majority of the more influential ancestors are sires, such that there are only 2 cows represented in the 25 ancestors with the highest impact on the breed. On the other hand, of the 671 founder sires, 24 Y chromosomes are currently represented in the reference population. One founder sire alone contributes nearly 60% of the Y chromosomes currently represented, such that the effective number of Y chromosomes is only 2.73.
Of the 6,171 founder cows (which were assumed to represent different mtDNA lineages), there are 2,435 mtDNA lineages represented in the reference population. The analysis of contributions of different mtDNA sources to the reference population indicates that the most influential founder cow was represented in 2.66% of the current mtDNA, whereas the effective number of mtDNA lineages was 578.2.
The degree of nonrandom selection and mating practiced in the population was evaluated by comparing the observed inbreeding in calves born in 2003 with the inbreeding that would be expected based on the average relationship among calves born in the same herd in the generation of the parents. This generation was considered to have been born in the same herd 6 yr earlier (i.e., the mean generation interval). The resulting relationship is illustrated in Figure 8, where the solid line represents the expected inbreeding for a given relationship, such that herds falling below the line have a lower than expected degree of inbreeding. Overall, 77% of the herds had lower than expected inbreeding, with a mean deviation by herd of –0.053 ± 0.071 between the observed inbreeding and the one that would be expected under random selection and mating. The correlations between herd size and the herd means for aij, Fi, and the difference (0.5 aij – Fi) were –0.15, –0.19, and 0.07, respectively. None of these correlations were significant (P > 0.1), suggesting that no clear relationship existed between herd size and the demographic parameters analyzed.
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DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and Alentejana is no longer threatened with extinction, as was feared a few years ago. Nevertheless, the development of the breed from a narrow base, and the strong influence of a few popular herds and sires, had inevitable consequences for genetic variability.
Monitoring the evolution of inbreeding and relationship over time has been the standard procedure to evaluate changes in genetic diversity of a population (Hill, 2000), and controlling the rate of inbreeding is usually one of the major targets in conservation and selection programs (Meuwissen and Woolliams, 1994; Caballero and Toro, 2002), and more so when selection decisions take family information into account, such as in BLUP (Villanueva et al., 2004). In recent years, parameters based on the probability of gene origin have been proposed as complementary indicators of inbreeding trends because they provide more insight into changes occurring in the population over a short period of time (Boichard et al., 1997). Under this perspective, the genetic composition of a breed may be assessed by analyzing the contributions of different herds (Robertson, 1953) and founders (James, 1972) to the current population. Lacy (1989) proposed the concept of effective number of founders as being the equivalent number of founders which, if they all had identical contributions, would be expected to generate the same genetic diversity as observed in the population under study. These principles were further developed by Boichard et al. (1997), who suggested the analysis of contributions of ancestors, and a corresponding effective number of ancestors, to evaluate the occurrence of bottlenecks in pedigrees. The above criteria have been applied in evaluating the genetic structure of cattle breeds in France (Boichard et al., 1996), Austria (Sölkner et al., 1998), Italy (Pérez Torrecillas et al., 2002), Spain (Gutiérrez et al., 2003), Ireland (McParland et al., 2007), United Kingdom (Roughsedge et al., 1999), and Denmark (Sorensen et al., 2005).
The level of pedigree completeness in Alentejana is quite acceptable, especially when compared with other breeds kept in similar extensive production systems, such as the Avileña-Negra Iberica (Gutiérrez et al., 2003). The current pedigree knowledge is nearly 4 equivalent generations for animals born in 2003. The length of productive life is an asset of this breed, but has resulted in long generation intervals on the dam paths of selection. On the other hand, bulls are used in reproduction for a long period of time (mean age at calves’ birth of 6.05 ± 2.35 yr), which will inevitably have an impact on the observed rate of inbreeding. Even though artificial insemination is very seldom used in Alentejana herds, a few popular bulls have a very large number of offspring by natural mating, such that 20% of the calves were produced by the 4% of the bulls siring more than 350 calves.
The more important feature of this study is the high rate and level of inbreeding found for the Alentejana breed (Table 2). The average inbreeding level in the current Alentejana population (F = 8.5% in calves born in 2003) is very high when compared with other beef (Cleveland et al., 2005; McParland et al., 2007) or dairy (Boichard et al., 1996; Roughsedge et al., 1999; Weigel, 2001; Kearney et al., 2004; Sorensen et al., 2005) cattle breeds, even though the majority of these breeds have more complete pedigree information. In addition, 12.5% of the calves in the Alentejana reference population have coefficients of inbreeding above 0.20 (results not shown). The percentage of inbred animals is now about 80% in Alentejana, which further indicates the need for urgent measures to be taken in order to slow the rate of inbreeding that has occurred in this population.
In Table 4, a summary of the major demographic parameters reported in the literature for several cattle breeds is presented, covering a wide range of management systems, census numbers, application of reproductive technologies, etc. When the results reported here are compared with those for other breeds, the annual rate of inbreeding (F = 0.33%/yr) in Alentejana is only lower than in Sayaguesa, similar to the rates found in Alistana, Asturiana de la Montaña, Morucha, and Mertolenga, and much higher than in dairy breeds, where artificial insemination is a common practice.
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; FAO, 1998) and in selection programs (Goddard and Smith, 1990), and represents a warning to reassess the management of the breed in the future.
The effective number of founders and ancestors in Alentejana (122 and 55, respectively) is not as dramatically low as for some of the other breeds summarized in Table 4, where the lowest values are observed for Mucca Pisana. However, the ratio fe/fa in Alentejana is about 2, indicating that bottlenecks have occurred in the pedigrees, as expected from the strong influence of a few prominent sires and herds. For example, the sire with the greatest influence on the breed is represented in 47% of the pedigrees of animals in the reference population. On the other hand, the heavy use of a limited number of sires and the emphasis on a few sire families has led to a very narrow representation of Y chromosomes (effective number less than 3) in the current population. The contribution of dams, as evaluated by the proportion of mtDNA founder sources currently represented, is a lot more diversified than that observed for Y chromosomes, with an effective number of mtDNA lineages of 578.2.
When rates of inbreeding and the influence of founders and ancestors are evaluated in Table 4, an interesting point arises. The effective number of ancestors and the rate of inbreeding both tend to be lower in dairy than in beef breeds, indicating that recent bottlenecks have occurred in dairy cattle, which are expected to be reflected as increased inbreeding in the long run, as suggested by Boichard et al. (1997).
The strong influence of a reduced number of Alentejana herds is demonstrated by the fact that 2 herds alone account for 24% of the gene pool, and the effective number of herds supplying great-grandsires is only 10. These results indicate that a selection nucleus has developed in the breed, and that most herds have been influenced by the selection practiced in this nucleus.
The average relationship among Alentejana animals from the same herd is quite high (0.33), and, if selection and mating were at random, would have resulted in even higher levels of inbreeding. Nevertheless, there are clear indications that producers are avoiding matings among more closely related individuals, such that the level of inbreeding is lower than expected if random selection and mating were practiced. On the other hand, the correlations of herd size with average relationship and mean inbreeding of the herd were not significant, suggesting that small herds have paid particular attention to managing inbreeding.
The average relationship among animals from different herds is only 0.02, but most herds have some relationship with the others, such that of the 5,151 mean relationships among the 102 herds in the reference population, less than 10% were zero. The low relationship among animals from different herds opens the possibility of migration between herds as a way to reduce inbreeding and maintain it at lower levels. In spite of the low average relationship among herds, a few influential herds have strong genetic connections with nearly all of the other herds, with a mean for the relationship of all herds with the 3 most influential herds of 0.043, reaching a maximum of 0.203. This represents an advantage from a genetic evaluation standpoint (Kennedy and Trus, 1993) but hampers the maintenance of genetic diversity in the long run.
The rate and level of inbreeding observed in Alentejana are among the highest reported for cattle breeds thus far. These trends clearly indicate that Alentejana is in a serious process of genetic erosion, and steps to control the rate of inbreeding are justified. Various methods of controlling inbreeding in selection programs have been suggested, including restrictions on family size, creation of sublines, optimized mating programs, restrictions on BLUP application, and appropriately weighting breeding value estimates and inbreeding generated by selection decisions (Sonesson et al., 2000; Weigel, 2001; Villanueva et al., 2004). For conservation programs, several approaches have also been suggested, including maximization of genetic contributions from different ancestors, recommendations on effective population size and generation intervals, use of molecular and pedigree information, etc. (Alderson, 1991; FAO, 1998; Fernández et al., 2005; Meuwissen, 2007; Woolliams, 2007). A combination of some of these methodologies, including rotation among families/herds, adequate mating strategies, and a combination of breeding value estimates and genetic contributions as the basis for selection decisions, should be implemented in order to avoid further losses of genetic variability in this breed.
In conclusion, pedigree analysis was useful in monitoring changes in population structure and gathering key demographic parameters in the Alentejana breed of cattle. Indicators of genetic erosion in this breed, such as the rate of inbreeding, are among the highest reported for commercial cattle breeds, and effective population size is far below the critical level generally recommended. Steps must be taken to avoid further losses in genetic variability in Alentejana, including selection of breeding animals with broader representation of ancestors and having a lower relationship with the population, rotation of animals among herds, and restrictions on BLUP-selection (e.g., based on the expected impact on inbreeding of the population).
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Footnotes |
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2 Corresponding author: genetica.ezn{at}mail.telepac.pt
Received for publication March 8, 2007. Accepted for publication August 3, 2007.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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