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Genetic diversity and population structure estimation of Brazilian Somali sheep from pedigree data
Small Ruminant Research 179 (2019) 64–69
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Genetic diversity and population structure estimation of Brazilian Somali sheep from pedigree data
T
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J.S. Figueredoa, , J.F. Cruzb, L.S. Sousaa, M.R. Teixeira Netoc, P.L.S. Carneirod, N.D. Britoe, R.G.S. Pinheiroe, K.S.O. Lacerdae, V.D. Mottina a
Pós-Graduação em Zootecnia, Universidade Estadual do Sudoeste da Bahia, Estrada Itapetinga-Itambé, Km 4, CEP 45.700-000, Brazil Departamento de Fitotecnia e Zootecnia, Universidade Estadual do Sudoeste da Bahia, Estrada do Bem Querer, km 4, Vitória da Conquista, Bahia, CEP 45083-900, Brazil c Colegiado de Medicina Veterinária, Faculdade de Tecnologia e Ciência, Rua Ubaldino Figueira, 200, CEP 45.020-510, Brazil d Departamento de Ciências Biológicas, Universidade Estadual do Sudoeste da Bahia, Rua José Moreira Sobrinho, CEP 45.206-190, Brazil e Colegiado de Agronomia, Universidade Estadual do Sudoeste da Bahia, Estrada do Bem Querer, km 4, Vitória da Conquista, Bahia, CEP 45083-900, Brazil b
A R T I C LE I N FO
A B S T R A C T
Keywords: Genetic conservation index Inbreeding Pedigree
The aim of this study was to describe and analyze the genetic diversity and population structure of Brazilian Somali sheep using pedigree records. Pedigree data of 9,038 individuals born between 1972 and 2018 were analyzed for completeness, gene origin probability, average relationship coefficient (AR), inbreeding coefficient, and genetic conservation index (GCI), using ENDOG v4.8 software. A total of 69.59%, 56.43%, 48.64%, 42.77%, and 34.05% of the examined individuals had pedigrees in the first, second, third, fourth and fifth ancestry, respectively. The total number of founders and ancestors was 833 and 837, whereas the effective number of founders and ancestors was 26 and 22, respectively. The eight main ancestors explained 51.04% of the total genetic variability. The AR and average inbreeding coefficient were 4.05 and 8.74, respectively. The mean GCI was 4.08, ranging from 1.00 to 17.43; three individuals showed a GCI above 17. In conclusion, the Brazilian Somali sheep show considerably high inbreeding coefficients, particularly those individuals born within the last decades. In contrast, some individuals have a high proportion of effective founders in their pedigrees, which can be used strategically for maintaining the genetic diversity of the breed.
1. Introduction In the late nineteenth and early twentieth centuries, several sheep breeds were introduced in Brazil and, due to natural selection, these breeds acquired specific characteristics of adaptations being considered local breeds, such as the Brazilian Somali sheep (Mariante et al., 2011). The Somali sheep, also referred to as blackhead Persian breed, originates from Somalia and belongs to the group of fat-rumped breeds (Porter, 2002). Its small body size and fat reserves in some body parts, particularly in the rump area, are adaptions that increase its survival arid regions (Magalhães et al., 2010). In the 1930s, Somali sheep were brought to Brazil by farmers from the coastal region; however, these animals were better adapted to the semi-arid conditions of northeastern Brazil (Paiva et al., 2011). As a result of random mating and natural selection over generations, the population acquired characteristics different from its original phenotypes, such as reduced fat accumulation on the rump, increased prolificity, and the presence of wool on the body (Santos, 2007). Officially
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termed Brazilian Somali, this breed is more rustic and has a lower nutritional requirement and lower production cost than other breeds introduced in Brazil (Magalhães et al., 2010). The population of Brazilian Somali sheep mainly consists of small herds belonging to research institutes and few herds belonging to breeders (Mariante et al., 2011; Paiva et al., 2011). Small and dispersed populations present a high risk of genetic drift and inbreeding depression, and consequently, extinction risk (Armstrong et al., 2006). The extinction of locally adapted breeds and its replacement by other more productive breeds represent a substantial loss of genetic diversity. The perception that genetic resources constitute a unique cultural and biological heritage emphasizes the need for measures to conserve these genetic groups (Barros et al., 2011). The maintenance of genetic diversity should be a key target for the conservation of populations at risk of extinction (Biagiotti et al., 2014). Pedigree data are evidence of the genetic and demographic structure over generations (Gutiérrez et al., 2003). The characterization of the genetic structure and genetic variability is strategic to evaluate the
Corresponding author. E-mail addresses: jenniferfi[email protected], [email protected] (J.S. Figueredo).
https://doi.org/10.1016/j.smallrumres.2019.09.010 Received 20 June 2018; Received in revised form 29 July 2019; Accepted 10 September 2019 Available online 11 September 2019 0921-4488/ © 2019 Elsevier B.V. All rights reserved.
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Fig. 1. Pedigree completeness of the Brazilian Somali sheep, with percentage of known ancestors up to the fifth ancestry.
parameter ƒe represents the number of founders whose contribution produced the same genetic variability as found in the study population (Boichard et al., 1997). The parameter ƒa is the minimum number of ancestors (whether they are founders or not) needed to explain the total genetic diversity of the study population (Sölkner et al., 1998). The top 500 founders and/or ancestors were sorted in descending order on the basis of their AR values and contribution, respectively, using the (SAS Institute Inc., 2003) SORT procedure in order to determine bottleneck effects. Spearman’s correlation of the PROC CORR of SAS v 9.1 (α = 0.01) was used for comparing the classifications of founders and ancestors. The GCI was calculated from the genetic contributions of all the founders, considering the proportion of genes of the founder animal in the animal pedigree under analysis, as described by Alderson et al. (1992).
occurrence of genetic erosion and facilitates extinction risk assessments of the breeds (Goyache et al., 2003; Oliveira et al., 2016). The aim of this study was to describe and analyze the genetic diversity and population structure of Brazilian Somali sheep based on pedigree data. 2. Materials and methods 2.1. Data Data were obtained from the Brazilian Association of Sheep Breeders and comprised 9,038 pedigrees of Brazilian Somali sheep born between 1972 and August 2018, from 130 herds in 18 Brazilian states; this total of animals/herds refers to a historical record since the formation of the breed. 2.2. Pedigree analysis
3. Results and discussion The software ENDOG v4.8 (Gutiérrez and Goyache, 2005) was used for pedigree analyses and estimation of population parameters. The following parameters were analyzed: pedigree completeness, average generation interval (GI), gene origin probability, average relationship coefficient (AR), inbreeding coefficient, effective population number, and genetic conservation index (GCI).
3.1. Pedigree completeness and demographic analysis Most of the Somalis sheep herds were unevenly distributed among states in the Brazilian semi-arid region. Moreover, herd sizes were considerably variable, with 52.11% of all individuals belonging to the 10 largest herds, which recorded, over the years, 1,662, 565, 558, 405, 391, 300, 245, 198, 194 and 192 animals, from highest to lowest, respectively. In contrast, the other 120 herds recorded, in the same period, 36 animals on average. The concentration of the population in the semi-arid region was most likely due to the breed’s adaption to the adverse climatic conditions. The variation in herd size, however, was probably a result of economic factors. Among the 9,038 analyzed pedigrees, 69.59% had known ancestors in the first, 56.43% in the second, 48.64% in the third, 42.77% in the fourth, and 34.05% in the fifth ancestries. The rate of increase of known ancestors in the pedigrees was 25.61%, 13.72%, 16.02%, and 23.32% from the fifth to the first ancestry, respectively (Fig. 1). Pedigree information is strategically important as it can be used to estimate population parameters; however, the accuracy of estimates depends on the completeness of the pedigrees (Teixeira Neto et al., 2012). The percentages of individuals with unknown ancestry in the first and fifth ancestries (30.41% and 65.95%, respectively) used in this study reflect the low level of pedigree completeness of Brazilian Somali sheep. The scarcity of information on more distant ancestors (as is common in pedigrees of production animals) may have led to an underestimation of inbreeding levels and AR (Boichard et al., 1997; Gowane et al., 2013). The averages of the maximum number of generations, complete generations, and equivalent generations were 4.02, 2.11, and 2.93, respectively. The number of equivalent generations was lower than that in Santa Inês sheep, which is the breed with the highest number of
2.2.1. Pedigree completeness and demographic analysis The level of pedigree completeness was evaluated by calculating the number of complete generations, maximum number of generations, and number of equivalent generations. The number of registered animals over a period of 47 years was determined. 2.2.2. Generation intervals and types of herds Generation intervals were calculated considering the four gametic pathways (father-son, father-daughter, mother-son, and motherdaughter). As suggested by Vassallo et al. (1986), the herds were ranked according to their organizational structure on the basis of their origin and use by the sires. 2.2.3. Genetic structure The algorithms proposed by Wright (1931) and Meuwissen and Luo (1992) were used to calculate the individual inbreeding coefficient (F) and inbreeding coefficient for the whole pedigree, respectively. The F statistics were obtained using the coefficients Fis, Fst, and Fit (Wright, 1965), and AR was calculated using the algorithm proposed by Quaas (1976). 2.2.4. Probability of gene origin and genetic conservation index The gene origin probability was estimated based on the effective number of founders (ƒe) and effective number of ancestors (ƒa). The 65
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Male
Female
Total
Number o f a ni ma l s
600 500 400 300 200 100 0
Registration Year Fig. 2. Number of Brazilian Somali sheep recorded in the Brazilian Association of Sheep Breeders (ARCO) database from 1972 to 2018.
3.2. Generation interval and types of herds
animals registered in Brazil (Teixeira Neto et al., 2013). Furthermore, the maximum number of generations and the number of equivalent generations were also lower than those in Iranian Zandi (GhafouriKesbi, 2010) and Baluchi sheep (Tahmoorespur and Sheikhloo, 2011), which are maintained in closed core populations. These comparative values demonstrate the scarcity of genealogical information on Brazilian Somali sheep. The number of registered animals was small in the first 13 years of breeding (1972–1984), with an average of 27 individuals per year. Over a period of 47 years, the highest number of animals within one year (n = 488) was recorded in 2001. However, there was a substantial reduction in the number of animals registered in the last seven years with an average of 112 individuals per year; in 2012, only 60 animals were registered. Similarly, in the last seven years, the numbers of herds that registered animals were 27, 26, 25, 21, 17, 14 and 13, respectively, showing a drastic and progressive reduction in the number of officially controlled individuals. A total of 65.47% of the entire registered population were females and 34.53% were males. The proportion of males:females was more distinguished in 2000 with 72.10% were females (Fig. 2). This skewed sex ratio is probably a consequence of a higher selection pressure on males as they are used to a lesser extent in mating systems. The trend of a female-biased sex ratio is also common in other sheep breeds (Barros et al., 2017; Rodrigues et al., 2009). This fact, however, is concerning for small populations due to the reducing number of registered male animals. The search for exotic breeds, considered more productive, such as the Dorper breed, officially introduced in Brazil in 1999 (SelaiveVillarroel and Osório, 2017), has contributed to reducing the registry of local genetic groups. However, domestic or naturalized breeds, such as Brazilian Somalis, are adapted to the environment where it is located, which a very favorable aspect that justifies its conservation. Farmers should be informed about this and other desirable characteristics and encouraged, through official programs, to maintain and work with these breeds. Likely, several live offspring may not necessarily be registered in the database of the breeders' association; however, the progressive reduction in the number of registered animals implies an effective decrease in the number of individuals. Ewes can be assumed to reproduce until six years of age; however, 2% of them may not reproduce, and the mortality rate is 10%, which leaves an estimated 367 ewes currently available for breeding. The same reasoning applied to the males, leaves to an estimated number of 268 rams currently available for breeding. However, the number of rams effectively used in mating has been low. Thus, the low number of ewes and the even fewer rams that genetically contributed result in considerably small effective population sizes, which reduce the genetic diversity of the breed.
The average GI was 3.53 ± 1.88 years, with similarity among the gametic passages father-son, father-daughter, mother-son, and motherdaughter, estimated at 3.52 ± 1.91, 3.51 ± 1.89, 3.43 ± 2.04 and 3.57 ± 1.85, respectively. The GI is influenced by the initial reproductive age of the rams and ewes, lambing interval, and the amount of time the animals are part of the herd (Teixeira Neto et al., 2013). In smaller populations at risk of extinction, the GI tends to be larger, such as in the Segureña and Morada Nova sheep with GI values of 3.79 (Barros et al., 2017) and 4.98 (Rodrigues et al., 2009), respectively. However, in larger populations, these values are generally lower, as in Santa Inês (Teixeira Neto et al., 2013) and Guilan sheep (Eteqadi et al., 2014), with GI values of 3.22 and 2.38, respectively. In genetic improvement programs, the GI should be maintained at around 3.0 years (Ghafouri-Kesbi, 2012). However, a higher GI may favor genetic diversity of breeds in conservation programs, as rams will be more likely to produce more descendants (Oliveira et al., 2016) as long as mating is controlled. GI higher for ewes (4.74) and lower for rams (2.8) was described in a Brazilian Somali herd (Paiva et al., 2011); these different results can be attributed, however, to the voluntary turnover of ewes and rams carried out on this herd - which belongs to a research institute. The average GI values for the different gametic passages confirmed in Brazilian Somali sheep are at an intermediate stage that allows improvement and maintenance of genetic variability. Most herds (78.46%) were classified as commercial herds, with 20.59% rated as commercial I, that used purchased or own rams but didn't sell them, and 79.41% as commercial II, which only used purchased rams and didn't sell them. The remaining 21.54% were multiplier herds, with 78.57% of type I, that used purchased or own rams and sold them, and 21.43% type II, which only used purchased rams and sold them. No isolated or nucleus-type herds were found (Table 1).
Table 1 Types of herds of the Brazilian Somali sheep according to their origin and way of use by the breeders.
66
Type of herd
Proportion (%)
Using purchased rams
Using own rams
Selling rams
Herd quantity
Multiplier I Multiplier II Commercial I Commercial II
16.92 4.62 16.15 62.31
Yes Yes Yes Yes
Yes No Yes No
Yes Yes No No
22 6 21 81
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F
AR
F (END)
30
F, AR a nd F end (%)
25 20 15 10 5 0
Year Fig. 3. Inbreeding (F), average relationship coefficient (AR), and inbreeding of endogamous animals (F(END)) values in Brazilian Somali sheep in the period 1988–2018.
Fig. 4. Individual and cumulative contributions of the ancestors and founders of greater importance to the genetic variability of the Brazilian Somali sheep.
2700
Number o f a nima ls
2400
2100 1800 1500 1200 900 600 300
0
Genetic Conservation Index Fig. 5. Number of animals of the Brazilian Somali sheep according to the genetic conservation index.
Oliveira et al., 2016; Rodrigues et al., 2009), as these values facilitate long-term inbreeding estimations (Goyache et al., 2010), with values above 2.1% considered high (Ghafouri-Kesbi, 2012). Different values as 0.17%, 2.1%, 3.87%, and 4.23% were described for the Mallorquina (Goyache et al., 2010), Afshari (Ghafouri-Kesbi, 2012), Santa Inês (Teixeira Neto et al., 2013), and Bharat Merino sheep (Gowane et al., 2013), respectively. The high AR value recorded in the present study suggests the need for a more rigorous control of mating, as high values indicate that some individual rams have been used more intensely. On
3.3. Genetic structure The AR changed over the years, with a low value (0.09%) in the first two decades of breed formation. Considering all individuals throughout the studied period the AR was 4.05%, and a gradual increase of 1.14% to 6.61% was observed from 1992 to 2008 when the highest individual AR (11.09%) was reached (Fig. 3). AR values are important in programs for the conservation and management of genetic diversity of populations (Mokhtari et al., 2013; 67
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3.4. Probability of gene origin and genetic conservation index
the other hand, rams with low AR may thus be used in targeted mating programs to increase the genetic variability of the breed. The inbreeding value (F) was zero in the first two decades. The value fluctuated from 1992 to 2006, but generally increased and reached 17.33% in 2006. From 2007, inbreeding declined to 9.34% in 2011. In 2012 and 2013, inbreeding increased substantially, reaching the highest level of the entire study period (16.67%), and remained above 10% in the last years (Fig. 3). In the initial phase of breed formation, “null" or very low values of inbreeding and AR followed by a subsequent increase appear to be a common phenomenon (Rodrigues et al., 2009; Goyache et al., 2010). It is noteworthy that the “null values” of inbreeding as reported in respective studies does not necessarily indicate the absence of inbreeding, but is merely a consequence of the unavailability of information on the previous generations, which prevents the calculation of these parameters. Over the 47 years of data on this breed, an average inbreeding coefficient of 8.74% was found. However, the last 17 years the average was 13.56%. Regardless of the scarcity of information on ancestral animals during the first 20 years of breed formation, 44.32% of the population (4.006 individuals) were inbred, with an average F value of 19.72%. Among the inbred individuals, 19.40% and 80.60% presented F values below and above 10.0%, respectively; it is noteworthy that 3.59% of these individuals had an F value above 40% (Fig. 3). It has been suggested that the average F values should below 10%, since higher values may predispose the population to inbreeding depression (Paiva et al., 2011), which may lead to a reduction in the average values of quantitative characters (Hussain et al., 2006; Selvaggi et al., 2010). The high values of inbreeding observed in Brazilian Somali sheep in recent years suggest mating among closely related individuals. It should be emphasized that the inbreeding values may be underestimated, considering the lack of information on the founder generations. The mean values of inbreeding were meaningly higher than those (0.54%) observed in a Brazilian Somalis herd kept under conservation (Paiva et al., 2011). Considering that the average level of inbreeding has remained considerably high (close to 10%), targeted mating using animals with a low AR value will contribute to keeping the level of inbreeding under control. When the level of inbreeding was considered to be associated with the number of complete generations - CG, the average inbreeding coefficient ranged from 0.26% (1 CG) to 24.96 (7 CG). Likewise, the percentage of inbred individuals ranged from 1.06% to 100%. These results differ those described by Paiva et al. (2011), using genetic markers in a herd kept for research purposes, in which as the number of traced generations increased, there was little change in inbreeding. Although the number of complete generations analyzed in both studies was different, the reason for this lower increase in inbreeding is certainly associated with the level of mating control. The Fit and Fis values were 0.068583 and –0.026855, respectively. The Fst value, which shows the genetic distance between subpopulations, was 0.092942, indicating moderate gene flow among the herds. A range of Fst values were reported in previous studies on Tunisian (0.030; Sassi-Zaidy et al., 2014), Sicilian (0.049; Tolone et al., 2012), Brazilian (0.200; Rodrigues et al., 2009), and Chinese native sheep (0.363; Wei et al., 2011). A low Fst value (Fst < 0.05) indicates high gene flow among the herds which may result from sharing of rams or the use of artificial insemination. In contrast, a high Fst value (Fst > 0.15) indicates a high subdivision of the population with no gene flow among herds. Consequently, an intermediate Fst value (0.05 < Fst < 0.15) suggests moderate gene flow among herds (Hartl et al., 2010). The non-use of artificial insemination and the lack of sharing rams have limited the connection of the herds; however, commercial exchange of offspring from purchased rams may explain the moderate gene flow regarding Fst values observed in the present study.
The ten main founders accounted for 37.19% of the genetic variability of the population. The four main founder males produced 161 offspring (F1) and accounted for 21.87% of the total breed variability (Fig. 4). The contribution made by founder animals depends on the number of descendants over generations (Teixeira Neto et al., 2013), and although the eighth main founder produced only one offspring (F1), this individual’s contribution was substantial (2.39%) due to the high number of further descendants. Thus, a larger number of founders leaving numerous descendants over several generations contributes to the maintenance of genetic variability (Barros et al., 2011; Goyache et al., 2003). The total number of founder individuals was 833 and the ƒe value was 26 (3.12%), which indicated a founder effect. The substantially smaller ƒe compared to the baseline population suggests that few rams were used and that the breed originated from a narrow genetic base (Barros et al., 2011; Gowane et al., 2013). A low number of founders is likely to produce a founder effect which reduces the effective population size and genetic variability within a population and increases homozygosity and loss of alleles due to genetic drift (Teixeira Neto et al., 2012). The number of ancestors was 837, the ƒa was 22 (2.63%), and the eight main ancestors (seven males and one female) accounted for 51.04% of the breed’s total genetic variability (Fig. 4). The contribution of these eight ancestors was considerably high compared with Spanish Segureña sheep (Barros et al., 2017), where 425 ancestors accounted for 50% of the population’s genetic variability. In Brazilian Somali sheep, the low number of ancestors explaining more than half of the genetic variation is likely a consequence of the small number of rams used over generations. Similar results were reported in a herd maintained at a research institute (Paiva et al., 2011). Thus, the use of rams from families different from those used previously is recommended to form new families within herds. The relationship between the effective number of founders and ancestors (ƒe/ƒa) was 1.18, despite the high correlation between the founding and ancestor animals (0.98; **P < 0.01), suggesting a discrete bottleneck effect. The ƒa value complement ƒe as it also considers the loss of genetic variability caused by the unbalanced use of rams (Gowane et al., 2014). It is noteworthy that the greater the distance between ƒe and ƒa is, the lower is the contribution of the founders over generations, producing a bottleneck effect. The ƒe value should be as small as possible, but ideally equal to ƒa (ƒe/ƒa = 1) (Boichard et al., 1997). The individual genetic conservation index ranged from 1 to 17.43, with an overall average of 4.08. Regarding sex, 39.71% of the females and 12.34% of the males presented an index of 1.0. Considering the entire population, 30.26% of the individuals presented an index of 1.0, and almost half (48.73%) presented an index ≤3.0. In contrast, 1.26% of the individuals presented an index > 13.0, and of these, 0.03% had a GCI > 17.0 (Fig. 5). Over the study period, GCI increased 0.22 for rams and 0.20 for ewes per year. In a Brazilian Somali herd kept for research purposes, an annual GCI growth rate of 0.31 and 0.28 was observed for rams and ewes, respectively (Paiva et al., 2011). The highest annual increase of GCI verified in the referred conservation herd concerning the total of recorded animals may be due to the more effective control of the mating, since a research institute manages this group of animals. In populations of conservation concern, maintenance of all alleles of the base population would be ideal; as this is practically not possible, it is advisable to carry out targeted mating using animals with a high GCI to ensure genetic variability. The GCI may be used for the selection of individuals or herds (Alderson et al., 1992; Paiva et al., 2011) which have a high proportion of founders in their pedigrees. In one of the subpopulations, which presented a mean GCI of 8.96, three individuals (one male and two females) with 65% of the effective founders (17/26) 68
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in their pedigrees were identified; these three individuals may be used in targeted mating aimed at maintaining alleles of the base population.
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A note on the population structure of the Avileña breed of cattle in Spain. Livest. Prod. Sc. 15, 285–288. https://doi.org/ 10.1016/0301-6226(86)90035-7. Wei, S., Hong, C., Hassan, M.H., Xin-Jun, L., Ming-Xing, C., James, K., 2011. Microsatellite-based genetic differentiation and phylogeny of sheep breeds in Mongolia sheep group of China. Agric. Sci. China 10, 1080–1087. https://doi.org/10. 1016/S1671-2927(11)60097-7. Wright, S., 1931. Evolution in mendelian populations. Genetics 16, 97–159. Wright, S., 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution (Nova York) 19, 395–420. https://doi.org/10. 2307/2406450.
4. Conclusion A substantial proportion of the Brazilian Somali sheep population showed considerably high inbreeding coefficients, and the average of this parameter has been above the recommended level over the past two decades. In contrast, the pedigree of several individuals contains a high proportion of effective founders; these animals could thus be used strategically for targeted mating to maintain the breed's genetic diversity. Therefore, the development and provision of a targeted mating scheme using rams with low AR and/or high GCI may contribute to the control or reduction of the current inbreeding levels. Declaration of Competing Interest None. Acknowledgements The authors would like to thank the CAPES (Coordination for the Improvement of Higher Level Personnel) for the financial support and the ARCO (Brazilian Association of Sheep Breeders) for supplying the data set. References Alderson, G.L.H., 1992. A system to maximize the maintenance of genetic variability in small populations. In: Alderson, L.J., Bodó, I. (Eds.), Genetic Conservation of Domestic Livestock. Cab International, Wallingford. Armstrong, E., Postiglioni, A., González, S., 2006. Population viability analysis of the Uruguayan Creole cattle genetic reserve. AGRI 38, 19–33. https://doi.org/10.1017/ S1014233900002029. Barros, E.A., Brasil, L.H.A., Tejero, J.P., Delgado-Bermejo, J.V., Ribeiro, M.N., 2017. Population structure and genetic variability of the Segureña sheep breed through pedigree analysis and inbreeding effects on growth traits. Small Rumin. Res. 149, 128–133. https://doi.org/10.1016/j.smallrumres.2017.02.009. Barros, E.A., Ribeiro, M.N., Almeida, M.J.O., Araújo, A.M., 2011. Population structure and genetic variability of the Marota goat breed. Archiv. Zootechnol. 60, 543–552. https://doi.org/10.1016/j.smallrumres.2017.02.009. Biagiotti, D., Guimarães, F.F., Sarmento, J.L.R., Santos, G.V., dos. Rego Neto, A.A., dos. Santos, N.P.S., Saraiva, T.T., Figueiredo Filho, L.A.S., Sena, L.S., 2014. Uso de estatística multivariada para estudo de caracterização racial em ovinos. Acta Technol. 9, 16–26. Boichard, D., Maignel, L., Verrier, E., 1997. The value of using probabilities of gene origin to measure genetic variability in a population. Genet. Sel. Evol. 29, 5–23. https://doi. org/10.1186/1297-9686-29-1-5. Eteqadi, B., Hossein-Sadeh, N.G., Shadparvar, A.A., 2014. Population structure and inbreeding effects on body weight traits of Guilan sheep in Iran. Small Rumin. Res. 119, 45–51. https://doi.org/10.1016/j.smallrumres.2014.03.003. Ghafouri-Kesbi, F., 2010. Analysis of genetic diversity in a close population of Zandi sheep using genealogical information. J. Genet. 89, 479–483. https://doi.org/10. 1007/s12041-010-0068-0. Ghafouri-Kesbi, F., 2012. Using pedigree information to study genetic diversity and reevaluating a selection program in an experimental flock of Afshari sheep. Arch. Tierzucht. 55, 375–384. https://doi.org/10.5194/aab-55-375-2012. Gowane, G.R., Chopra, A., Misra, S.S., Prince, L.L.L., 2014. Genetic diversity of a nucleus flock of Malpura sheep through pedigree analyses. Small Rumin. Res. 120, 35–41. https://doi.org/10.1016/j.smallrumres.2014.04.016. Gowane, G.R., Prakash, V., Chopra, A., Prince, L.L.L., 2013. Population structure and effect of inbreeding on lamb growth in Bharat Merino sheep. Small Rumin. Res. 114, 72–79. https://doi.org/10.1016/j.smallrumres.2013.06.002. Goyache, F., Gutiérrez, J.P., Fernández, I., Gómez, E., Alvarez, I., Díez, J., Royo, L.J., 2003. Using pedigree information to monitor genetic variability of endangered populations: the Xalda sheep breed of Asturias as an example. J. Anim. Breed. Genet. 120, 95–105. https://doi.org/10.1046/j.1439-0388.2003.00378.x. Goyache, F., Fernández, I., Espinosa, M.A., Payeras, L., Pérez-Pardal, L., Gutiérrez, J.P., Royo, L.J., Alvarez, I., 2010. Análisis demográfico y genético de la raza ovina Mallorquina. ITEA 106, 3–14.
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Genetic diversity and population structure estimation of Brazilian Somali sheep from pedigree data
T
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J.S. Figueredoa, , J.F. Cruzb, L.S. Sousaa, M.R. Teixeira Netoc, P.L.S. Carneirod, N.D. Britoe, R.G.S. Pinheiroe, K.S.O. Lacerdae, V.D. Mottina a
Pós-Graduação em Zootecnia, Universidade Estadual do Sudoeste da Bahia, Estrada Itapetinga-Itambé, Km 4, CEP 45.700-000, Brazil Departamento de Fitotecnia e Zootecnia, Universidade Estadual do Sudoeste da Bahia, Estrada do Bem Querer, km 4, Vitória da Conquista, Bahia, CEP 45083-900, Brazil c Colegiado de Medicina Veterinária, Faculdade de Tecnologia e Ciência, Rua Ubaldino Figueira, 200, CEP 45.020-510, Brazil d Departamento de Ciências Biológicas, Universidade Estadual do Sudoeste da Bahia, Rua José Moreira Sobrinho, CEP 45.206-190, Brazil e Colegiado de Agronomia, Universidade Estadual do Sudoeste da Bahia, Estrada do Bem Querer, km 4, Vitória da Conquista, Bahia, CEP 45083-900, Brazil b
A R T I C LE I N FO
A B S T R A C T
Keywords: Genetic conservation index Inbreeding Pedigree
The aim of this study was to describe and analyze the genetic diversity and population structure of Brazilian Somali sheep using pedigree records. Pedigree data of 9,038 individuals born between 1972 and 2018 were analyzed for completeness, gene origin probability, average relationship coefficient (AR), inbreeding coefficient, and genetic conservation index (GCI), using ENDOG v4.8 software. A total of 69.59%, 56.43%, 48.64%, 42.77%, and 34.05% of the examined individuals had pedigrees in the first, second, third, fourth and fifth ancestry, respectively. The total number of founders and ancestors was 833 and 837, whereas the effective number of founders and ancestors was 26 and 22, respectively. The eight main ancestors explained 51.04% of the total genetic variability. The AR and average inbreeding coefficient were 4.05 and 8.74, respectively. The mean GCI was 4.08, ranging from 1.00 to 17.43; three individuals showed a GCI above 17. In conclusion, the Brazilian Somali sheep show considerably high inbreeding coefficients, particularly those individuals born within the last decades. In contrast, some individuals have a high proportion of effective founders in their pedigrees, which can be used strategically for maintaining the genetic diversity of the breed.
1. Introduction In the late nineteenth and early twentieth centuries, several sheep breeds were introduced in Brazil and, due to natural selection, these breeds acquired specific characteristics of adaptations being considered local breeds, such as the Brazilian Somali sheep (Mariante et al., 2011). The Somali sheep, also referred to as blackhead Persian breed, originates from Somalia and belongs to the group of fat-rumped breeds (Porter, 2002). Its small body size and fat reserves in some body parts, particularly in the rump area, are adaptions that increase its survival arid regions (Magalhães et al., 2010). In the 1930s, Somali sheep were brought to Brazil by farmers from the coastal region; however, these animals were better adapted to the semi-arid conditions of northeastern Brazil (Paiva et al., 2011). As a result of random mating and natural selection over generations, the population acquired characteristics different from its original phenotypes, such as reduced fat accumulation on the rump, increased prolificity, and the presence of wool on the body (Santos, 2007). Officially
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termed Brazilian Somali, this breed is more rustic and has a lower nutritional requirement and lower production cost than other breeds introduced in Brazil (Magalhães et al., 2010). The population of Brazilian Somali sheep mainly consists of small herds belonging to research institutes and few herds belonging to breeders (Mariante et al., 2011; Paiva et al., 2011). Small and dispersed populations present a high risk of genetic drift and inbreeding depression, and consequently, extinction risk (Armstrong et al., 2006). The extinction of locally adapted breeds and its replacement by other more productive breeds represent a substantial loss of genetic diversity. The perception that genetic resources constitute a unique cultural and biological heritage emphasizes the need for measures to conserve these genetic groups (Barros et al., 2011). The maintenance of genetic diversity should be a key target for the conservation of populations at risk of extinction (Biagiotti et al., 2014). Pedigree data are evidence of the genetic and demographic structure over generations (Gutiérrez et al., 2003). The characterization of the genetic structure and genetic variability is strategic to evaluate the
Corresponding author. E-mail addresses: jenniferfi[email protected], [email protected] (J.S. Figueredo).
https://doi.org/10.1016/j.smallrumres.2019.09.010 Received 20 June 2018; Received in revised form 29 July 2019; Accepted 10 September 2019 Available online 11 September 2019 0921-4488/ © 2019 Elsevier B.V. All rights reserved.
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Fig. 1. Pedigree completeness of the Brazilian Somali sheep, with percentage of known ancestors up to the fifth ancestry.
parameter ƒe represents the number of founders whose contribution produced the same genetic variability as found in the study population (Boichard et al., 1997). The parameter ƒa is the minimum number of ancestors (whether they are founders or not) needed to explain the total genetic diversity of the study population (Sölkner et al., 1998). The top 500 founders and/or ancestors were sorted in descending order on the basis of their AR values and contribution, respectively, using the (SAS Institute Inc., 2003) SORT procedure in order to determine bottleneck effects. Spearman’s correlation of the PROC CORR of SAS v 9.1 (α = 0.01) was used for comparing the classifications of founders and ancestors. The GCI was calculated from the genetic contributions of all the founders, considering the proportion of genes of the founder animal in the animal pedigree under analysis, as described by Alderson et al. (1992).
occurrence of genetic erosion and facilitates extinction risk assessments of the breeds (Goyache et al., 2003; Oliveira et al., 2016). The aim of this study was to describe and analyze the genetic diversity and population structure of Brazilian Somali sheep based on pedigree data. 2. Materials and methods 2.1. Data Data were obtained from the Brazilian Association of Sheep Breeders and comprised 9,038 pedigrees of Brazilian Somali sheep born between 1972 and August 2018, from 130 herds in 18 Brazilian states; this total of animals/herds refers to a historical record since the formation of the breed. 2.2. Pedigree analysis
3. Results and discussion The software ENDOG v4.8 (Gutiérrez and Goyache, 2005) was used for pedigree analyses and estimation of population parameters. The following parameters were analyzed: pedigree completeness, average generation interval (GI), gene origin probability, average relationship coefficient (AR), inbreeding coefficient, effective population number, and genetic conservation index (GCI).
3.1. Pedigree completeness and demographic analysis Most of the Somalis sheep herds were unevenly distributed among states in the Brazilian semi-arid region. Moreover, herd sizes were considerably variable, with 52.11% of all individuals belonging to the 10 largest herds, which recorded, over the years, 1,662, 565, 558, 405, 391, 300, 245, 198, 194 and 192 animals, from highest to lowest, respectively. In contrast, the other 120 herds recorded, in the same period, 36 animals on average. The concentration of the population in the semi-arid region was most likely due to the breed’s adaption to the adverse climatic conditions. The variation in herd size, however, was probably a result of economic factors. Among the 9,038 analyzed pedigrees, 69.59% had known ancestors in the first, 56.43% in the second, 48.64% in the third, 42.77% in the fourth, and 34.05% in the fifth ancestries. The rate of increase of known ancestors in the pedigrees was 25.61%, 13.72%, 16.02%, and 23.32% from the fifth to the first ancestry, respectively (Fig. 1). Pedigree information is strategically important as it can be used to estimate population parameters; however, the accuracy of estimates depends on the completeness of the pedigrees (Teixeira Neto et al., 2012). The percentages of individuals with unknown ancestry in the first and fifth ancestries (30.41% and 65.95%, respectively) used in this study reflect the low level of pedigree completeness of Brazilian Somali sheep. The scarcity of information on more distant ancestors (as is common in pedigrees of production animals) may have led to an underestimation of inbreeding levels and AR (Boichard et al., 1997; Gowane et al., 2013). The averages of the maximum number of generations, complete generations, and equivalent generations were 4.02, 2.11, and 2.93, respectively. The number of equivalent generations was lower than that in Santa Inês sheep, which is the breed with the highest number of
2.2.1. Pedigree completeness and demographic analysis The level of pedigree completeness was evaluated by calculating the number of complete generations, maximum number of generations, and number of equivalent generations. The number of registered animals over a period of 47 years was determined. 2.2.2. Generation intervals and types of herds Generation intervals were calculated considering the four gametic pathways (father-son, father-daughter, mother-son, and motherdaughter). As suggested by Vassallo et al. (1986), the herds were ranked according to their organizational structure on the basis of their origin and use by the sires. 2.2.3. Genetic structure The algorithms proposed by Wright (1931) and Meuwissen and Luo (1992) were used to calculate the individual inbreeding coefficient (F) and inbreeding coefficient for the whole pedigree, respectively. The F statistics were obtained using the coefficients Fis, Fst, and Fit (Wright, 1965), and AR was calculated using the algorithm proposed by Quaas (1976). 2.2.4. Probability of gene origin and genetic conservation index The gene origin probability was estimated based on the effective number of founders (ƒe) and effective number of ancestors (ƒa). The 65
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Male
Female
Total
Number o f a ni ma l s
600 500 400 300 200 100 0
Registration Year Fig. 2. Number of Brazilian Somali sheep recorded in the Brazilian Association of Sheep Breeders (ARCO) database from 1972 to 2018.
3.2. Generation interval and types of herds
animals registered in Brazil (Teixeira Neto et al., 2013). Furthermore, the maximum number of generations and the number of equivalent generations were also lower than those in Iranian Zandi (GhafouriKesbi, 2010) and Baluchi sheep (Tahmoorespur and Sheikhloo, 2011), which are maintained in closed core populations. These comparative values demonstrate the scarcity of genealogical information on Brazilian Somali sheep. The number of registered animals was small in the first 13 years of breeding (1972–1984), with an average of 27 individuals per year. Over a period of 47 years, the highest number of animals within one year (n = 488) was recorded in 2001. However, there was a substantial reduction in the number of animals registered in the last seven years with an average of 112 individuals per year; in 2012, only 60 animals were registered. Similarly, in the last seven years, the numbers of herds that registered animals were 27, 26, 25, 21, 17, 14 and 13, respectively, showing a drastic and progressive reduction in the number of officially controlled individuals. A total of 65.47% of the entire registered population were females and 34.53% were males. The proportion of males:females was more distinguished in 2000 with 72.10% were females (Fig. 2). This skewed sex ratio is probably a consequence of a higher selection pressure on males as they are used to a lesser extent in mating systems. The trend of a female-biased sex ratio is also common in other sheep breeds (Barros et al., 2017; Rodrigues et al., 2009). This fact, however, is concerning for small populations due to the reducing number of registered male animals. The search for exotic breeds, considered more productive, such as the Dorper breed, officially introduced in Brazil in 1999 (SelaiveVillarroel and Osório, 2017), has contributed to reducing the registry of local genetic groups. However, domestic or naturalized breeds, such as Brazilian Somalis, are adapted to the environment where it is located, which a very favorable aspect that justifies its conservation. Farmers should be informed about this and other desirable characteristics and encouraged, through official programs, to maintain and work with these breeds. Likely, several live offspring may not necessarily be registered in the database of the breeders' association; however, the progressive reduction in the number of registered animals implies an effective decrease in the number of individuals. Ewes can be assumed to reproduce until six years of age; however, 2% of them may not reproduce, and the mortality rate is 10%, which leaves an estimated 367 ewes currently available for breeding. The same reasoning applied to the males, leaves to an estimated number of 268 rams currently available for breeding. However, the number of rams effectively used in mating has been low. Thus, the low number of ewes and the even fewer rams that genetically contributed result in considerably small effective population sizes, which reduce the genetic diversity of the breed.
The average GI was 3.53 ± 1.88 years, with similarity among the gametic passages father-son, father-daughter, mother-son, and motherdaughter, estimated at 3.52 ± 1.91, 3.51 ± 1.89, 3.43 ± 2.04 and 3.57 ± 1.85, respectively. The GI is influenced by the initial reproductive age of the rams and ewes, lambing interval, and the amount of time the animals are part of the herd (Teixeira Neto et al., 2013). In smaller populations at risk of extinction, the GI tends to be larger, such as in the Segureña and Morada Nova sheep with GI values of 3.79 (Barros et al., 2017) and 4.98 (Rodrigues et al., 2009), respectively. However, in larger populations, these values are generally lower, as in Santa Inês (Teixeira Neto et al., 2013) and Guilan sheep (Eteqadi et al., 2014), with GI values of 3.22 and 2.38, respectively. In genetic improvement programs, the GI should be maintained at around 3.0 years (Ghafouri-Kesbi, 2012). However, a higher GI may favor genetic diversity of breeds in conservation programs, as rams will be more likely to produce more descendants (Oliveira et al., 2016) as long as mating is controlled. GI higher for ewes (4.74) and lower for rams (2.8) was described in a Brazilian Somali herd (Paiva et al., 2011); these different results can be attributed, however, to the voluntary turnover of ewes and rams carried out on this herd - which belongs to a research institute. The average GI values for the different gametic passages confirmed in Brazilian Somali sheep are at an intermediate stage that allows improvement and maintenance of genetic variability. Most herds (78.46%) were classified as commercial herds, with 20.59% rated as commercial I, that used purchased or own rams but didn't sell them, and 79.41% as commercial II, which only used purchased rams and didn't sell them. The remaining 21.54% were multiplier herds, with 78.57% of type I, that used purchased or own rams and sold them, and 21.43% type II, which only used purchased rams and sold them. No isolated or nucleus-type herds were found (Table 1).
Table 1 Types of herds of the Brazilian Somali sheep according to their origin and way of use by the breeders.
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Type of herd
Proportion (%)
Using purchased rams
Using own rams
Selling rams
Herd quantity
Multiplier I Multiplier II Commercial I Commercial II
16.92 4.62 16.15 62.31
Yes Yes Yes Yes
Yes No Yes No
Yes Yes No No
22 6 21 81
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F
AR
F (END)
30
F, AR a nd F end (%)
25 20 15 10 5 0
Year Fig. 3. Inbreeding (F), average relationship coefficient (AR), and inbreeding of endogamous animals (F(END)) values in Brazilian Somali sheep in the period 1988–2018.
Fig. 4. Individual and cumulative contributions of the ancestors and founders of greater importance to the genetic variability of the Brazilian Somali sheep.
2700
Number o f a nima ls
2400
2100 1800 1500 1200 900 600 300
0
Genetic Conservation Index Fig. 5. Number of animals of the Brazilian Somali sheep according to the genetic conservation index.
Oliveira et al., 2016; Rodrigues et al., 2009), as these values facilitate long-term inbreeding estimations (Goyache et al., 2010), with values above 2.1% considered high (Ghafouri-Kesbi, 2012). Different values as 0.17%, 2.1%, 3.87%, and 4.23% were described for the Mallorquina (Goyache et al., 2010), Afshari (Ghafouri-Kesbi, 2012), Santa Inês (Teixeira Neto et al., 2013), and Bharat Merino sheep (Gowane et al., 2013), respectively. The high AR value recorded in the present study suggests the need for a more rigorous control of mating, as high values indicate that some individual rams have been used more intensely. On
3.3. Genetic structure The AR changed over the years, with a low value (0.09%) in the first two decades of breed formation. Considering all individuals throughout the studied period the AR was 4.05%, and a gradual increase of 1.14% to 6.61% was observed from 1992 to 2008 when the highest individual AR (11.09%) was reached (Fig. 3). AR values are important in programs for the conservation and management of genetic diversity of populations (Mokhtari et al., 2013; 67
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3.4. Probability of gene origin and genetic conservation index
the other hand, rams with low AR may thus be used in targeted mating programs to increase the genetic variability of the breed. The inbreeding value (F) was zero in the first two decades. The value fluctuated from 1992 to 2006, but generally increased and reached 17.33% in 2006. From 2007, inbreeding declined to 9.34% in 2011. In 2012 and 2013, inbreeding increased substantially, reaching the highest level of the entire study period (16.67%), and remained above 10% in the last years (Fig. 3). In the initial phase of breed formation, “null" or very low values of inbreeding and AR followed by a subsequent increase appear to be a common phenomenon (Rodrigues et al., 2009; Goyache et al., 2010). It is noteworthy that the “null values” of inbreeding as reported in respective studies does not necessarily indicate the absence of inbreeding, but is merely a consequence of the unavailability of information on the previous generations, which prevents the calculation of these parameters. Over the 47 years of data on this breed, an average inbreeding coefficient of 8.74% was found. However, the last 17 years the average was 13.56%. Regardless of the scarcity of information on ancestral animals during the first 20 years of breed formation, 44.32% of the population (4.006 individuals) were inbred, with an average F value of 19.72%. Among the inbred individuals, 19.40% and 80.60% presented F values below and above 10.0%, respectively; it is noteworthy that 3.59% of these individuals had an F value above 40% (Fig. 3). It has been suggested that the average F values should below 10%, since higher values may predispose the population to inbreeding depression (Paiva et al., 2011), which may lead to a reduction in the average values of quantitative characters (Hussain et al., 2006; Selvaggi et al., 2010). The high values of inbreeding observed in Brazilian Somali sheep in recent years suggest mating among closely related individuals. It should be emphasized that the inbreeding values may be underestimated, considering the lack of information on the founder generations. The mean values of inbreeding were meaningly higher than those (0.54%) observed in a Brazilian Somalis herd kept under conservation (Paiva et al., 2011). Considering that the average level of inbreeding has remained considerably high (close to 10%), targeted mating using animals with a low AR value will contribute to keeping the level of inbreeding under control. When the level of inbreeding was considered to be associated with the number of complete generations - CG, the average inbreeding coefficient ranged from 0.26% (1 CG) to 24.96 (7 CG). Likewise, the percentage of inbred individuals ranged from 1.06% to 100%. These results differ those described by Paiva et al. (2011), using genetic markers in a herd kept for research purposes, in which as the number of traced generations increased, there was little change in inbreeding. Although the number of complete generations analyzed in both studies was different, the reason for this lower increase in inbreeding is certainly associated with the level of mating control. The Fit and Fis values were 0.068583 and –0.026855, respectively. The Fst value, which shows the genetic distance between subpopulations, was 0.092942, indicating moderate gene flow among the herds. A range of Fst values were reported in previous studies on Tunisian (0.030; Sassi-Zaidy et al., 2014), Sicilian (0.049; Tolone et al., 2012), Brazilian (0.200; Rodrigues et al., 2009), and Chinese native sheep (0.363; Wei et al., 2011). A low Fst value (Fst < 0.05) indicates high gene flow among the herds which may result from sharing of rams or the use of artificial insemination. In contrast, a high Fst value (Fst > 0.15) indicates a high subdivision of the population with no gene flow among herds. Consequently, an intermediate Fst value (0.05 < Fst < 0.15) suggests moderate gene flow among herds (Hartl et al., 2010). The non-use of artificial insemination and the lack of sharing rams have limited the connection of the herds; however, commercial exchange of offspring from purchased rams may explain the moderate gene flow regarding Fst values observed in the present study.
The ten main founders accounted for 37.19% of the genetic variability of the population. The four main founder males produced 161 offspring (F1) and accounted for 21.87% of the total breed variability (Fig. 4). The contribution made by founder animals depends on the number of descendants over generations (Teixeira Neto et al., 2013), and although the eighth main founder produced only one offspring (F1), this individual’s contribution was substantial (2.39%) due to the high number of further descendants. Thus, a larger number of founders leaving numerous descendants over several generations contributes to the maintenance of genetic variability (Barros et al., 2011; Goyache et al., 2003). The total number of founder individuals was 833 and the ƒe value was 26 (3.12%), which indicated a founder effect. The substantially smaller ƒe compared to the baseline population suggests that few rams were used and that the breed originated from a narrow genetic base (Barros et al., 2011; Gowane et al., 2013). A low number of founders is likely to produce a founder effect which reduces the effective population size and genetic variability within a population and increases homozygosity and loss of alleles due to genetic drift (Teixeira Neto et al., 2012). The number of ancestors was 837, the ƒa was 22 (2.63%), and the eight main ancestors (seven males and one female) accounted for 51.04% of the breed’s total genetic variability (Fig. 4). The contribution of these eight ancestors was considerably high compared with Spanish Segureña sheep (Barros et al., 2017), where 425 ancestors accounted for 50% of the population’s genetic variability. In Brazilian Somali sheep, the low number of ancestors explaining more than half of the genetic variation is likely a consequence of the small number of rams used over generations. Similar results were reported in a herd maintained at a research institute (Paiva et al., 2011). Thus, the use of rams from families different from those used previously is recommended to form new families within herds. The relationship between the effective number of founders and ancestors (ƒe/ƒa) was 1.18, despite the high correlation between the founding and ancestor animals (0.98; **P < 0.01), suggesting a discrete bottleneck effect. The ƒa value complement ƒe as it also considers the loss of genetic variability caused by the unbalanced use of rams (Gowane et al., 2014). It is noteworthy that the greater the distance between ƒe and ƒa is, the lower is the contribution of the founders over generations, producing a bottleneck effect. The ƒe value should be as small as possible, but ideally equal to ƒa (ƒe/ƒa = 1) (Boichard et al., 1997). The individual genetic conservation index ranged from 1 to 17.43, with an overall average of 4.08. Regarding sex, 39.71% of the females and 12.34% of the males presented an index of 1.0. Considering the entire population, 30.26% of the individuals presented an index of 1.0, and almost half (48.73%) presented an index ≤3.0. In contrast, 1.26% of the individuals presented an index > 13.0, and of these, 0.03% had a GCI > 17.0 (Fig. 5). Over the study period, GCI increased 0.22 for rams and 0.20 for ewes per year. In a Brazilian Somali herd kept for research purposes, an annual GCI growth rate of 0.31 and 0.28 was observed for rams and ewes, respectively (Paiva et al., 2011). The highest annual increase of GCI verified in the referred conservation herd concerning the total of recorded animals may be due to the more effective control of the mating, since a research institute manages this group of animals. In populations of conservation concern, maintenance of all alleles of the base population would be ideal; as this is practically not possible, it is advisable to carry out targeted mating using animals with a high GCI to ensure genetic variability. The GCI may be used for the selection of individuals or herds (Alderson et al., 1992; Paiva et al., 2011) which have a high proportion of founders in their pedigrees. In one of the subpopulations, which presented a mean GCI of 8.96, three individuals (one male and two females) with 65% of the effective founders (17/26) 68
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in their pedigrees were identified; these three individuals may be used in targeted mating aimed at maintaining alleles of the base population.
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4. Conclusion A substantial proportion of the Brazilian Somali sheep population showed considerably high inbreeding coefficients, and the average of this parameter has been above the recommended level over the past two decades. In contrast, the pedigree of several individuals contains a high proportion of effective founders; these animals could thus be used strategically for targeted mating to maintain the breed's genetic diversity. Therefore, the development and provision of a targeted mating scheme using rams with low AR and/or high GCI may contribute to the control or reduction of the current inbreeding levels. Declaration of Competing Interest None. Acknowledgements The authors would like to thank the CAPES (Coordination for the Improvement of Higher Level Personnel) for the financial support and the ARCO (Brazilian Association of Sheep Breeders) for supplying the data set. References Alderson, G.L.H., 1992. A system to maximize the maintenance of genetic variability in small populations. In: Alderson, L.J., Bodó, I. (Eds.), Genetic Conservation of Domestic Livestock. Cab International, Wallingford. Armstrong, E., Postiglioni, A., González, S., 2006. Population viability analysis of the Uruguayan Creole cattle genetic reserve. AGRI 38, 19–33. https://doi.org/10.1017/ S1014233900002029. Barros, E.A., Brasil, L.H.A., Tejero, J.P., Delgado-Bermejo, J.V., Ribeiro, M.N., 2017. Population structure and genetic variability of the Segureña sheep breed through pedigree analysis and inbreeding effects on growth traits. Small Rumin. Res. 149, 128–133. https://doi.org/10.1016/j.smallrumres.2017.02.009. Barros, E.A., Ribeiro, M.N., Almeida, M.J.O., Araújo, A.M., 2011. Population structure and genetic variability of the Marota goat breed. Archiv. Zootechnol. 60, 543–552. https://doi.org/10.1016/j.smallrumres.2017.02.009. Biagiotti, D., Guimarães, F.F., Sarmento, J.L.R., Santos, G.V., dos. Rego Neto, A.A., dos. Santos, N.P.S., Saraiva, T.T., Figueiredo Filho, L.A.S., Sena, L.S., 2014. Uso de estatística multivariada para estudo de caracterização racial em ovinos. Acta Technol. 9, 16–26. Boichard, D., Maignel, L., Verrier, E., 1997. The value of using probabilities of gene origin to measure genetic variability in a population. Genet. Sel. Evol. 29, 5–23. https://doi. org/10.1186/1297-9686-29-1-5. Eteqadi, B., Hossein-Sadeh, N.G., Shadparvar, A.A., 2014. Population structure and inbreeding effects on body weight traits of Guilan sheep in Iran. Small Rumin. Res. 119, 45–51. https://doi.org/10.1016/j.smallrumres.2014.03.003. Ghafouri-Kesbi, F., 2010. Analysis of genetic diversity in a close population of Zandi sheep using genealogical information. J. Genet. 89, 479–483. https://doi.org/10. 1007/s12041-010-0068-0. Ghafouri-Kesbi, F., 2012. Using pedigree information to study genetic diversity and reevaluating a selection program in an experimental flock of Afshari sheep. Arch. Tierzucht. 55, 375–384. https://doi.org/10.5194/aab-55-375-2012. Gowane, G.R., Chopra, A., Misra, S.S., Prince, L.L.L., 2014. Genetic diversity of a nucleus flock of Malpura sheep through pedigree analyses. Small Rumin. Res. 120, 35–41. https://doi.org/10.1016/j.smallrumres.2014.04.016. Gowane, G.R., Prakash, V., Chopra, A., Prince, L.L.L., 2013. Population structure and effect of inbreeding on lamb growth in Bharat Merino sheep. Small Rumin. Res. 114, 72–79. https://doi.org/10.1016/j.smallrumres.2013.06.002. Goyache, F., Gutiérrez, J.P., Fernández, I., Gómez, E., Alvarez, I., Díez, J., Royo, L.J., 2003. Using pedigree information to monitor genetic variability of endangered populations: the Xalda sheep breed of Asturias as an example. J. Anim. Breed. Genet. 120, 95–105. https://doi.org/10.1046/j.1439-0388.2003.00378.x. Goyache, F., Fernández, I., Espinosa, M.A., Payeras, L., Pérez-Pardal, L., Gutiérrez, J.P., Royo, L.J., Alvarez, I., 2010. Análisis demográfico y genético de la raza ovina Mallorquina. ITEA 106, 3–14.
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