CC BY
21
Ukrainian Journal of Ecology
Ukrainian Journal ofEcology, 2019,9(1), 251-261
ORIGINAL ARTICLE UDC 636.4.082.25:575.22
Assessing genomic taurine/zebuine admixture in the southern meat cattle based on microsatellite markers
A.S. Kramarenko, O.I. Karatieieva, A.V. Lykhach, S.I. Lugovoy, V.Ya. Lykhach, T.V. Pidpala, L.S.
Patryeva, S.S. Kramarenko
Mykolayiv National Agrarian University, Georgiy Gongadze Str., 9, Mykolayiv, 54020 Ukraine. E-mail:
[email protected] Received: 12.02.2019. Accepted: 20.03.2019
Hybridization between wild and domestic bovine species occurs worldwide either spontaneously or by organized crossing. The Southern Meat (SM) cattle is a composite developed by crossing Cuban zebu (Bos indicus) with different cattle breeds (Bos taurus) - local Red Steppe, Hereford, Charolais, Santa Gertrudis, Dairy Shorthorn. The main aim of this work was to study the genetic structure of the Southern Meat breed (SM) cattle and to assess the taurine/zebuine admixture in the SM population using microsatellites. A set of 192 heifers representing the SM cattle (the 'Askaniiske' State Pilot Farm, Kherson region, Ukraine) was included in the study during 2013-2014. Based on the origin of the individuals studied, all heifers were attributed to two groups according to the different degree of Zebu blood: the LZ group (< 3/8 percent Zebu blood; n=100) and the UZ group (>3/8 percent Zebu blood; n=92). Ten bovine autosomal polymorphic microsatellite loci (BM1818, BM1824, BM2113, ETH3, ETH10, INRA023, TGLA53, TGLA122, TGLA227 and SPS115) were genotyped to estimate various parameters of genetic diversity. The total number of genotype estimates ranged substantially over loci from 18 (locus BM1824) to 37 (locus INRA023), giving a mean number of 27.9 ± 1.96 genotypes per locus. Overall, one hundred and four alleles were observed across the 10 microsatellite markers examined, with allelic diversity (the average number of observed alleles per locus) of 10.4 ± 0.76. Significant difference (P<0.05-0.001) was found between the LZ and UZ groups with regard to distribution of allele frequencies across all loci. The values of Ae, Ho, He and Fis in two SM cattle groups did not differ significantly (a non-parametric paired Wilcoxon's test; for all cases P>0.05). At each locus some alleles were identified that were present at higher frequencies in the LZ group and absent or present at relatively lower frequencies in the UZ group, or vice versa. Evidence for an association between specific alleles at every locus with B.indicus/B.taurus breed was assessed by using a Logistic Regression model. Significant relationship was discovered only for two loci, TGLA227 (^=22.30; P<0.001) and ETH10 (^=27.70; P<0.001). It can be assumed that the TGLA227 (77 bp) and ETH10 (209-211 bp) alleles among the SM cattle examined individuals were inherited from a B.indicus ancestor. On the other hand, the TGLA227 (89 bp) and ETH10 (217-219 bp) alleles which prevails among individuals in the LZ group were inherited from a B.taurus ancestor. Thus, the SM cattle presented with high level of taurine/zebuine admixture, which is consistent with the breeding history.
Keywords: Bos indicus; Bos taurus; hybridization; southern meat cattle; taurine/zebuine admixture; microsatellite markers
Introduction
Hybridization between species may occur if closely related species share an overlapping habitat or through human intervention during captive breeding. Uncontrolled hybridization, as it occurs in nature, may have had a significant impact on the formation of domestic breeds, but can also affect the genetic integrity of domestic and wild species. Monitoring the species composition of these animals may become essential for the future preservation of genetic diversity (Nijman et al., 2003).
Ongoing hybridization that results in admixture of parental genes from 2 different species and introgression (i.e., transfer of genes from one species to another by repeated backcrossing), can cause the native population to be replaced by one genetically and phenotypically resembling the nonnative form in some traits (Huxel, 1999).
Hybridization between wild and domesticated forms has been documented: in canids between coyotes (Canis latrans) and domestic dogs (Canis familiaris) in the USA (Adams et al., 2000); in felids between domestic cats (Felis silvestris catus) and African wildcats (Felis silvestris lybica) (Le Roux et al., 2015) or European wildcats (Nussberger et al., 2013); in suids between wild boars (Sus scrofa) and domestic pigs (Sus scrofa domestica) in Bulgaria (Nikolov et al., 2017), in Belgium and Luxembourg (Frantz et al., 2013); in birds between wild common quails (Coturnix coturnix) and domesticated Japanese quails (Coturnix japónica) in France (Charaza et al., 2010). Hybridization and high degree of genetic introgression has been observed between wild and domesticated reindeer populations (Rangifer tarandus) (Kharzinova et al., 2016).
Hybridization between wild and domestic bovine species occurs worldwide either spontaneously or by organized crossing (Nijman et al., 2002). Within the group of the Bovini several hybrids have been described: a cross of banteng (Bos javanicus) and zebu (Bos indicus) (Nijman et al., 2002; Hartati et al., 2015); a cross of yak (Poephagus grunniens) and taurine cattle (Tumennasan et al., 1997; Luo et al., 2014); the North-American beefalo, a cross of taurine cattle (Bos taurus) and the American bison (Bison bison) (Polziehn et al., 1995; Halber et al., 2005). In Africa, introgression of Indian zebu bulls (Bos indicus) in taurine herds occurs and has improved the tolerance of the cattle (Bos taurus) to hot and dry environments (Bradley et al., 1994). Bongso et al. (1988) described a spontaneous hybridization of wild gaur (Bos gaurus) and zebu (Bos indicus). The Southern Meat cattle is a composite developed by crossing Cuban zebu (Bos indicus) with different cattle breeds (Bos taurus) - local Red Steppe, Hereford, Charolais, Santa Gertrudis, Dairy Shorthorn. The Southern Meat breed is the fourth in representation among Ukrainian breeding achievements of meat production. The body shape similar to zebu, coat mainly red. External features include the strong constitution, light bones, balanced body shape, well-shaped muscles of the hip and shoulder, long thorax, especially in the rump part. The head is light with large jowl, topline straight, tough limbs, skin smooth and flexible. The breed is well adapted to hot climate and extreme conditions of the steppes. It is resistant to diseases. The growth intensity is high as well as the meat yield and good quality of beef. The roughage is used effectively. Body weight of cows is 580-620 kg and weight of bulls is 900-1100 kg (Pilarczyk et al., 2015; Suprun et al., 2016).
The use of molecular markers has increased the ability to identify species, subspecies and populations and different molecular markers (e.g. microsatellite DNA loci) also have been used to detect, quantify and to determine the age of hybridization and introgression events in wild (Rodriguez et al., 2008) and captive-reared animals (Nijman et al., 2003; Lecis et al., 2006; Kharzinova et al., 2016).
Several DNA markers are now available to analyse the genetic background of hybrid Bovini. Mitochondrial DNA (D-loop) markers and cytochrome-b typing reveal introgression via the maternal lineage (Verkaar et al, 2003; Nijman et al., 2003). The species origin of the nuclear genome can be inferred from species-specific microsatellite alleles (Frisch et al., 1997; MacHugh et al., 1997), AFLP patterns (Buntjer et al., 2002) or mutations in satellite DNA.
Nijman et al. (1999) has shown that amplified fragment length polymorphisms (AFLP) correlated with introgression of zebu (Bos indicus) in African cattle populations. While, a cattle-specific mtDNA control region fragment and cattle-specific alleles at three autosomal microsatellite loci (ILSTS013, ILSTS050 and SPS115) has been used by Qi et al. (2010) for a diagnostic approach to assess the impact of cattle introgression on domestic yak populations. Moreover, a panel of 54,609 SNPs (50k) was used to genetically characterize Indonesian Peranakan Ongole cattle by comparison with B. taurus, B. indicus, B. javanicus and composite B. taurus x B. indicus breeds (Hartati et al., 2015).
The main aim of this work was to study the genetic structure of the Southern Meat breed (SM) cattle and to assess the taurine/zebuine admixture in the SM population using microsatellites.
Materials and methods
A set of 192 heifers representing the SM cattle (the 'Askaniiske' State Pilot Farm, Kherson region, Ukraine) was included in the study during 2013-2014. The animals were unrelated and randomly selected from herd.
Based on the origin of the individuals studied, all heifers were attributed to two groups according to the different degree of Zebu blood: the LZ group (< 3/8 percent Zebu blood; n=100) and the UZ group (>3/8 percent Zebu blood; n=92). Total genomic DNA was extracted from tissue samples using Nexttec column (Nexttec Biotechnology GmbH, Germany) following the manufacturer's instructions. The DNA concentration was estimated by measuring the absorbance at 260 nm and the DNA quality was checked by separation on agarose gels.
Ten bovine autosomal polymorphic microsatellite loci (BM1818, BM1824, BM2113, ETH3, ETH10, INRA023, TGLA53, TGLA122, TGLA227 and SPS115) were genotyped to estimate various parameters of genetic diversity.
Microsatellites were amplified in two multiplex reactions. Electrophoresis was carried out using an ABI 3130xl Genetic Analyzer (Applied Biosystems, USA). Allele sizes of each microsatellite marker were determined using GeneMapper ver. 4.0 (Applied Biosystems).
For each group (LZ and UZ) we calculated the total number of genotypes (TNG), number of singleton genotypes (NGS) and number of unique genotypes (NGU), i.e., variants that were encountered in a single sample set for each microsatellite locus. The two-way ANOVA (for qualitative traits) was used for the evaluation of differences in the NGS and NGU frequency between the SM cattle groups and across the microsatellite loci.
GenAIEx v.6.5 software (Peakall and Smouse, 2012) was used to estimate basic population genetic descriptive statistics for each marker in the two SM cattle groups: the allelic frequencies, total number of alleles (TNA), effective number of alleles (Ae), number of private alleles, most frequent alleles with frequencies higher than 0.2 (MFA), observed (Ho) and expected heterozygosity (He), fixation indices (Fis).
Significant differences of all genetic descriptive statistics in the two SM cattle groups were obtained through a non-parametric paired Wilcoxon's test using the PAST software (Hammer et al., 2001).
Deviations from Hardy-Weinberg equilibrium (HWE) were performed for each locus using the Pearson's chi-square goodness-of-fit test using the GenAIEx v.6.5 software.
Significant differences of genotype and allelic frequencies in two SM cattle groups were determined from the contingency tables 2xk (where k is the total number of genotypes or the total number of alleles) in terms of chi-square (x2) and the Monte Carlo significance test procedure (with 100000 random permutations) was used in the PAST software (Hammer et al., 2001).
Results
The total number of genotypes, the number of singleton genotypes and the number of unique genotypes per locus in the two SM cattle groups (LZ and UZ) are given in Table 1. First, we show that the TNG estimates ranged substantially over loci from 18 (locus BM1824) to 37 (locus INRA023), giving a mean number of 27.9 ± 1.96 genotypes per locus. Significant differences over loci were also found in the NGS frequency (F9;399=2.23; P=0.019). A two-way ANOVA revealed significant main effect for the SM cattle group in the NGU frequency (F1;538=4.39; P=0.037). Additionally, there was a significant interaction between microsatellite markers and the SM cattle groups (F9;538=2.57; P=0.007).
Table 1. The total number of genotypes (TNG), number of singleton genotypes (NGS) and number of unique genotypes (NGU), i.e., variants that were encountered in a single sample set at the 10 microsatellite loci in the two SM cattle groups.
Locus n TNG NGS NGU X (Pmc)
LZ UZ LZ UZ
TGLA227 146 34 44105 13/27 7 14 50.64 (<0.01)
BM2113 191 28 43282 45536 4 10 86.65 (<0.001)
TGLA53 109 25 42248 44075 5 10 41.78 (<0.001)
ETH10 192 25 44774 45170 2 3 47.83 (<0.001)
SPS115 192 19 42826 42064 4 2 28.89 (<0.001)
TGLA122 192 31 45597 46569 4 7 91.42 (<0.001)
INRA023 192 37 44013 16/32 5 17 88.83 (<0.001)
BM1818 189 32 46204 43922 12 6 94.12 (<0.001)
ETH3 168 30 13/22 44105 10 8 55.39 (<0.001)
BM1824 192 18 42095 43802 6 3 72.33 (<0.001)
n represents sample size;x2 (PMC) is chi-square test and the Monte Carlo significance test procedure (with 100,000 random permutations).
Secondly, the unique genotypes were more abundant in the LZ group for loci BM1818, ETH3 and BM1824 than in the UZ group. On the other hand, for loci TGLA227, BM2113, TGLA53 and INRA023 the unique genotypes were more relatively plentiful in the UZ group than in the LZ group (Table 1).
Significant difference (PMC<0.01-0.001) was found between the LZ and UZ groups with regard to the distribution of genotypes across all microsatellite markers (Table 1).
Overall, one hundred and four alleles were observed across the 10 microsatellite markers examined, with allelic diversity (the average number of observed alleles per locus) of 10.4 ± 0.76. When analyzing the two SM cattle groups separately, the number alleles per locus ranged from seven (locus BM1824) to 12 (locus TGLA53) with a mean of 9.1 ± 0.53 for the LZ group, and from seven (loci BM1824 and SPS115) to 14 (locus TGLA227) with a mean of 9.4 ± 0.69 for the UZ group (Table 2).
Table 2. The total number of alleles (TNA), group-private and most frequent alleles (with frequencies higher than 0.2) at the 10 microsatellite loci in the two SM cattle groups._
Locus TNA Private alleles, bp MFA, bp X2 (Pmc)
LZ UZ LZ UZ LZ UZ
TGLA227 11 14 103 79, 85, 99, 101 77, 89 77 40.14 (<0.001)
BM2113 9 9 131 127 125 135 80.68 (<0.001)
TGLA53 12 11 168, 184 154 156, 164 156, 162 46.99 (<0.001)
ETH10 8 8 225 223 209, 211, 217 209, 217 35.27 (<0.001)
SPS115 8 7 244 - 248, 250 248, 250 16.88 (<0.05)
TGLA122 8 9 - 141 143, 151 149 81.38 (<0.001)
INRA023 9 10 - 196 202, 214 214 75.59 (<0.001)
BM1818 8 8 272 274 264, 268 262, 266 101.17 (<0.001)
ETH3 11 11 101, 131 109, 113 117, 121 115, 117 38.32 (<0.001)
BM1824 7 7 184 190 180 180, 182 86.65 (<0.001)
MFA - the most frequent alleles.x2 (PMC) is chi-square test and the Monte Carlo significance test procedure (with 100000 random permutations). Group-specific alleles are indicated in bold.
A total of 23 group-private alleles were found in the SM cattle, 10 were identified in the LZ group, while 13 were detected in the UZ group (Table 2). Significant difference (PMC<0.05-0.001) was also found between the LZ and UZ groups with regard to distribution of allele frequencies across all loci (Table 2). The TGLA227 (77 bp), TGLA53 (156 bp), ETH10 (209 and 217 bp), SPS115 (248 and 250 bp), INRA023 (214 bp), ETH3 (117 bp) and BM1824 (180 bp) alleles of the microsatellite markers were predominant in the LZ group as well as in heifers of the UZ group. On the other hand, 17 group-specified alleles (with frequencies higher than 0.2) were found for the nine microsatellite loci (except at the SPS115 locus) in the SM cattle, 10 were only detected in the LZ group, while 7 were only observed in the UZ group (Table 2).
Figure 1. Allelic frequency distribution across the 10 microsatellite markers in the LZ (1) and UZ (2) groups. Frequency of alleles marked with *, ** and *** was significantly different between groups (* P<0.05; ** P<0.01; *** P<0.001).
Allele frequency profiles for each of the microsatellite marker in the two SM cattle groups and alleles with the statistically significant differences in frequencies between the comparing groups are shown in Figure 1.
A high disparity in microsatellite allelic distribution between the LZ and UZ groups was observed. At each locus some alleles were identified that were present at higher frequencies in the LZ group and absent or present at relatively lower frequencies in the UZ group, or vice versa.
The effective number of alleles (Ae), the observed (Ho) and expected heterozygosity (He), and fixation indices (Fis) across the 10 microsatellite markers in the two SM cattle groups are shown in Table 3.
Average effective numbers of alleles were 3.90 ± 0.26 and 4.61 ± 0.34 per locus in different cattle groups. In the LZ group the markers with the highest Ho values were BM1818, followed by ETH10, and in the UZ group the markers with the highest Ho values were BM2113 and TGLA122. The expected heterozigosities across the LZ and UZ groups varied from 0.656 (locus BM1824) to 0.818 (locus BM1818) and from 0.626 (locus BM1824) to 0.845 (locus TGLA53), respectively.
Of the 10 microsatellite markers, the fixation indices of TGLA227, TGLA53, ETH3 and BM1824 loci were positive and significantly different from 0 (P<0.05) in the LZ group as well as in heifers of the UZ group. The average Fis values were 0.114 ± 0.070 and 0.096 ± 0.051 in the two SM cattle groups, respectively.
Table 3. The effective allele numbers (Ae), heterozygosity (Ho - observed, He - expected) and within-population inbreeding
estimates (Fis) at the 10 microsatellite loci in the two SM cattle groups._
Locus Ae Ho He Fis
LZ UZ LZ UZ LZ UZ LZ UZ
TGLA227 4.25 4.36 0.649 0.609 0.765 0.771 0.151 # 0.210 #
BM2113 3.16 5.22 0.717 0.859 0.684 0.808 -0.049 -0.062
TGLA53 3.2 6.46 0.351 0.481 0.688 0.845 0.490 # 0.431 #
ETH10 4.95 4.58 0.81 0.793 0.798 0.782 -0.015 -0.015
SPS115 4.17 3.45 0.72 0.717 0.76 0.71 0.053 # -0.01
TGLA122 3.59 5.82 0.73 0.859 0.721 0.828 -0.012 -0.037
INRA023 3.64 4.75 0.74 0.772 0.725 0.79 -0.02 0.023
BM1818 5.43 4.38 0.867 0.769 0.816 0.772 -0.063 0.003
ETH3 3.7 4.37 0.329 0.566 0.729 0.771 0.548 # 0.266 #
BM1824 2.91 2.67 0.62 0.533 0.656 0.626 0.055 # 0.149
Mean 3.9 4.61 0.653 0.696 0.734 0.77 0.114 0.096
SE ± 0.26 ± 0.34 ± 0.057 ± 0.044 ± 0.016 ± 0.020 ± 0.070 ± 0.051
# Loci shoving significant deviation from Hardy-Weinberg equilibrium. SE - standard error.
The values of Ae, Ho, He and Fis in two SM cattle groups did not differ significantly (a non-parametric paired Wilcoxon's test; for all cases P>0.05). Table 4 lists the high-frequency alleles in the different breeds of zebu (Asian, African and South American origin) and beef cattle (European origin) across the 10 microsatellite markers used. A literature review was carried out across publications (research papers and PhD theses) on the genetic diversity of the zebu and beef cattle breeds based on the microsatellite loci from our list.
Evidence for an association between specific alleles at every locus with B. indicus/B. taurus breed was assessed by using a Logistic Regression model. Significant relationship was discovered only for two loci, TGLA227 (^=22.30; P<0.001) and ETH10 (X2=27.70; P<0.001).
Locus TGLA227: Short alleles (77 and 79 bp) were found more often among B.indicus breeds, while long alleles (89 and 91 bp) were common in the B.taurus breeds (Table 4, Figure 2A). Thus, it can be assumed that the TGLA227 (77 bp) allele among the SM cattle examined individuals was inherited from a B.indicus ancestor (Figure 1).
On the other hand, the TGLA227 (89 bp) allele which prevails among individuals in the LZ group was inherited from a B.taurus ancestor (Table 2).
Locus ETH10: Short alleles (209 and 211 bp) were found more often among B.indicus breeds, while long alleles (217 and 219 bp) were common in B.taurus breeds (Table 4, Figure 2B). This suggests that the ETH10 (209-211 bp) alleles in the SM cattle examined individuals were inherited from a B.indicus ancestor and the ETH10 (217-219 bp) alleles which dominate among individuals in the LZ group were inherited from a B.taurus ancestor (Figure 1, Table 2).
Discussion
Two hundred and seventy-nine genotypes were detected from the 10 microsatellite markers surveyed in the SM cattle population, yielding a mean value of 27.9 genotypes per locus. In a Sicilian cattle population studied by Cosenza et al. (2015), TGLA53 locus has shown the highest total number of genotypes (TNG=89), while the lowest TNG was 15 in BM1824, and the average was 47.18, i.e. at least than double the population of the SM cattle. In the Ongole Grade cattle (the Indonesian native beef cattle, B.indicus), all the microsatellite loci (TGLA227, ETH225, BM1824, INRA005 and MM12) showed a genotype variation except for the TGLA227 locus in which all samples were uniformly (Saturano, 2018).
For the Nellore cattle (Brazil, B.indicus) ninety-four alleles were detected from the 10 loci surveyed, yielding a mean value of 9.4 alleles per locus. The TGLA227 locus had one allele with a much higher frequency than the other alleles (75 bp) and the ETH10 locus had two alleles with high frequencies (207-209 bp).
Table 4. A list of the high-frequency alleles in different zebu and the beef cattle (Ch - Charolais, Her - Hereford, Sim -Simmental) breeds across the 10 microsatellite markers._
Bree d Locus
TGLA2 27 BM2113 TGLA53 ETH10 SPS115 TGLA1 22 INRA0 23 BM18 18 ETH3 BM1824
Zebua 79, 81 131, 143 159, 167 210, 212, 214 247, 255 137, 149 215 113, 115 183
Zebu b 77 129, 135, 141 209, 213 246, 248 143, 153 214 180, 182
Zebuc 77 123, 131 158 209 239, 241, 243 141, 143 208 111 180
Zebu d 77, 81 141 160, 168 209, 213 246, 248, 250 137, 151 214 115, 117 180, 182
Zebue 77 129, 139, 141 160, 168 209, 211, 213 246, 248 137, 151 214 115, 117 180, 182
Zebuf 77, 79 157 209, 211, 213 246 153 214 115
Zebug 75 129, 141 160 207, 209 137 214, 216 115, 117 178, 180, 182
Zebu h 77, 87 135, 137, 141 209, 2013 246 133, 141 198, 214 180
Zebu h 77, 79 135, 139 209 248 143 198, 214 180, 182, 192
Zebu h 77, 79 129, 135, 139 217 248, 256 143 208, 214 180, 182, 192
Chi 89 131 217 248 151 206 262 117 182
Chj 83, 89, 91 131, 135 217 248 143, 151 202, 206 117, 125 280, 282, 288
Chk 131, 133 151, 153, 157 209, 211, 215 203, 205, 207, 209 178, 180, 182, 184
Her' 91, 93, 95 133, 139 160, 162 219, 221, 223 248 143, 153 206, 216 117, 119 180, 182, 184
Herj 89, 91 135, 139 217, 219 248, 260 143 214 117, 119 182
Herm 94 218, 220, 222
Simn 80 128 164 214 242 150 208, 212, 214 112, 114, 124 182, 188
Siml 81 131 217 248 151 214 268 117 188
Simo 81 131, 139 168 217 248, 256 143, 151 214 117, 127 180, 188
a) Kesvulu et al., 2009; b) Bicalho et al., 2006; c) Escobar et al., 2009; d) Novoa, Usaquen, 2010; e) Gomez et al., 2013; f) Egito et al., 2007; g) Cervini et al., 2006; h) Hussein, 2008; i) Putnova et al., 2011; j) Kundrat, 2007; k) Sifuentes-Rincon et al., 2007; l) Janik et al., 2002; m) Yoon et al., 2005; n) Stevanovic et al., 2009; o) Choroszy et al., 2006.
The mean observed heterozygosity value was 0.564 (from 0.323 to 0.847) and the mean expected heterozygosity value was 0.679 (from 0.422 to 0.855). A total, eight loci recorded positive inbreeding coefficients indicating presence of inbreeding with respect to these loci and the overall mean inbreeding coefficient (Fis) for this zebu population was 0.164 (Cervini et al., 2006). Egito et al. (2007) showed that among the Brazilian zebuine breeds (Gyr, Guzerat and Nellore) the mean allele number was very similar - 8.4-8.8 alleles per locus, while the two domesticated taurine breeds (Holstein and Jersey) were less diverse with a smaller average number of alleles slightly above 8.0.
The mean observed heterozigozity values ranged from 0.636 to 0.654 and from 0.632 to 0.685 for the zebuine and taurine breeds, respectively. In all breeds observed heterozygosity values were nominally smaller than the expected ones. Highest values of Fis were seen for Jersey (0.121) followed closely by the three zebuine breeds Gyr (0.120), Guzerat (0.113) and Nellore (0.096).
In the Punganur cattle (India, B. indicus), a total of 66 alleles were produced by eleven markers with a mean of 6.0 alleles per locus, the overall mean observed and expected heterozygosities were 0.684 and 0.666, respectively, and the overall mean coefficient of inbreeding (Fis) was -0.001 and it ranged from -0.225 to 0.512 (Kesvulu et al., 2009).
Escobar et al. (2009), identified the genetic variability of the zebu (B.indicus) herd with the Brahman (Red and White) and Gyr breeds in Colombia, detecting that one hundred and fifty seven alleles were detected from the 11 loci surveyed, yielding a mean value of 14.3 alleles per locus. The overall mean observed heterozygocity was 0.706, and the mean expected heterozygocity was 0.777.
In other Colombian Brahman (B. indicus) population (Novoa, Usaquen, 2010) the number of alleles per locus (TNA) fluctuated between 5 and 12 with an average of 7.9, and the inbreeding coefficient (Fis) was positive, low for the whole population (0.067), and significantly different from zero, suggesting a deficit of heterozygotes in the sample. The overall mean expected and observed heterozygosity values were 0.637 and 0.667, respectively.
Eleven microsatellites were used to evaluate the genetic variation from three populations of Charolais cattle (B. taurus) located in northeast Mexico (Sifuentes-Rincon et al., 2007). Twelve alleles per loci was the average. Allele number per locus ranged from 7 alleles in ETH10 locus, to 18 alleles in TGLA53. The allele diversity was similar among the ranches. Expected heterozygocity was higher than the observed for all loci in the three ranches. The overall mean heterozygocity was 0.500. Observed heterozygosity ranged from 0.388 to 0.780, from 0.235 to 0.816, and from 0.230 to 0.732 for ranches 1, 2, and 3, respectively.
MacHugh et al. (1998) reported a value of heterozygosity for Charolais of 0.525, and Maudet et al. (2002) found a heterozygosity of 0.640 in Charolais in France. These heterozygocity values are similar than those estimated by Sifuentes-Rincon et al. (2007), suggesting the genetic diversity of Charolais in Mexico is comparable to that reported in Europe.
Alleles (bp)
1.0 0.8
J? 0 6
_Q
re
"8 04 a
0.2 0.0
205 207 209 211 213 215 217 219 221 223 225 Alleles (bp)
Figure 2. Logistic Regression results: A - locus TGLA22; B - locus ETH10. Model displays the probability of outcome (0 -B.indicus, 1 - B.taurus) versus significant predictor variable (allele length).
In the Serbian population of Simmental cattle (B. taurus) a total of 92 alleles were detected and the mean number of alleles (TNA) per locus was 8.4 (Stevanovic et al., 2009). The most polymorphic microsatellite were TGLA53 (14 alleles), TGLA227 (11 alleles) and INRA023 (11 alleles) loci. In addition, Ho values ranged from 0.452 to 0.774, with overall mean value of 0.662, whilst He values varied from 0.557 to 0.893, with an average of 0.753. Overall, microsatellite DNA markers analysed in the Serbian population of Simmental cattle appeared more polymorphic than in other breeds of Simmental cattle (from Poland, Slovakia, Czech Republic) (Janik et al., 2001; Choroszy et al., 2006; Czernekova et al., 2006).
The mean TNA per locus observed in Serbian population of Simmental cattle (8.3) is higher than 7.27 found in Simmental cattle from Poland (Choroszy et al., 2006). Moreover, the total number of alleles we observed in Serbian population of Simmental cattle (92) is higher than Janik et al. (2001) and Choroszy et al. (2006) found in Simmental cattle from Poland for the same set of microsatellite loci (79 and 80, respectively).
Putnova et al. (2011) reported that in the Czech beef cattle (B.taurus) populations the mean number of allele per each locus ranged from 4 to 11 with a mean of 7.4 for Charolais and 5.8 for Simmental. All the analyzed loci showed high polymorphism and sufficient informativeness, though ETH10 in Charolais cattle showed very low heterozygosity. The highest polymorphism for TGLA227 and INRA023 loci had also been found by Radko et al. (2005) in Polish Red cattle and Hereford. Table 5 presents a list of B.indicus- and B.taurus-specific alleles across the different microsatellite loci. The two groups (zebu and B.taurus) breeds have shown separate and characteristic distributions of alleles in ETH225 locus tested (Table 5). Alleles with high molecular weight (154, 158 and 160 bp) were more frequent in zebu animals while taurine animals exhibited low weight (< 150 bp) (Hall, Bradley, 1995).
Ukrainian Journal of Ecology' 258 Table 5. A list of B. indicus- and B. taurus-specific alleles across the different microsalellite loci._
Locus / alleles Species Literature
ETH225 (154, 158 and 160 bp) B. indicus Hall, Bradley, 1995
ETH152 (191 and 193 bp); ILSTS001 (77 bp); ETH225; B. indicus MacHugh et al., 1997
HEL1; HRHl; ILSTS005; ILSTS014; OCAM (182 bp); RASA;
TGIA48
ETH10 (207, 209 and 211 bp); ETH152 (191 bp); ETH225 B. indicus Loftus et al., 1999
(153, 155, 157 and 159 bp); Hel13; ILSTS005; INRA005
INRA124 (130 bp) B. indicus Hanotte et al., 2000
INRA189 (88 bp), BMS861 (156 bp) B. indicus Edwards et al., 2000
BM2113; ILSTS001 B. indicus Magee et al., 2002
BM2113 (130 and 142 bp); CSSM66 (181 bp); ETH10 (207, B. indicus (Asian) Ibeagha-Awemu et al., 2004
209 and 211 bp); ETH152 (191 bp); HEL1 (101, 107 and
117 bp); HEL13 (182 and 186 bp); TGLA122 (144 bp).
ETH225 (153, 157, 159 bp); TGLA227 (79 bp); TGLA122 B. indicus Liron et al., 2006
(136 bp)
TGLA227 (77 and 79 bp) B. indicus our results
ETH10 (209 and 211 bp) B. indicus our results
ETH225 (144, 146, 148 and 150 bp) B. taurus Hall, Bradley, 1995
INRA124 (132 bp) B. taurus Hanotte et al., 2000;
INRA189 (98 bp) B. taurus Edwards et al., 2000
(European)
BMS861 (158 bp) B. taurus Edwards et al., 2000
BM1824 (189 bp); CSSM66 (183 bp); B. taurus Ibeagha-Awemu et al., 2004
ETH10 (215 bp); HEL1 (113 bp); (European)
HEL13 (188 bp); ILSTS6 (289 bp);
TGLA122 (150 bp).
BM1824 (181 bp); BM2113 (122 bp); B. taurus Ibeagha-Awemu et al., 2004
ETH10 (219 bp); ETH152 (195 bp); (African)
HEL1 (109 bp); HEL13 (190 bp);
INRA023 (199 bp).
TGLA227 (89 and 91 bp) B. taurus our results
ETH10 (217 and 219 bp) B. taurus our results
As suggested by MacHugh et al. (1997), substantial differences in the distribution of alleles at 10 microsatellite loci have been observed between zebu and taurine cattle: ETH152 (191 and 193 bp), ILSTS001 (77 bp), ETH225, HEL1, HRHl, ILSTS005, ILSTS014, OCAM (182 bp), RASA and TGIA48. In total, 18 alleles from the 10 diagnostic loci were classified as zebu-diagnostic. On the other hand, six microsatellite loci - ETH10 (207, 209 and 211 bp), ETH152 (191 bp), ETH225 (153, 155, 157 and 159 bp), HEL13, ILSTS005 and INRA005 - displayed alleles that were present at high frequency in the Asian zebu populations (Table 5). In total, 13 alleles from the six loci were classified as diagnostic of zebu ancestry (Loftus et al., 1999). A Y-specific (INRA124) microsatellite polymorphism has been recently described (Hanotte et al. 2000). This locus shows two alleles. The 132 bp allele is specific to cattle of taurine origin (African or European taurine) and the 130 bp allele is specific to cattle of indicine origin (Hanotte et al., 2000).
Additionally, both BM861 (a similar marker to INRA124) and INRA189 loci seem to show allele size variants specific to taurine and zebu in the cattle breeds studied (Edwards et al., 2000). The BM2113 and ILSTS001 loci have been described previously as displaying a total of four alleles specific to West African B.taurus breeds (MacHugh et al., 1997), whereas three alleles across the HEL1 and ILSTS001 loci are considered to be exclusive to populations exhibiting B.indicus ancestry (Magee et al., 2002). Ibeagha-Awemu et al. (2004) reported that microsatellite allelic distribution displayed groups of alleles specific to the Indian zebu, African taurine and European taurine. Zebu alleles were identified at seven of the ten loci and their mean frequency distribution was the highest in Indian zebus (63.1%) followed by African zebus (45.2%) while being less than 10.0% in both African and European taurines. Identified European taurine specific alleles were seven at seven loci (see Table 5). Their distribution was the highest as expected in the European taurines (32.5%) while being less than 4.0% in breeds in the other bio-geographical groups.
Conclusion
In this study we used microsatellite data to study the genetic constitution of the SM cattle by considering introgression of B. indicus and B. taurus. In the SM cattle zebu and taurine alleles were identified at two of the 10 loci studied, TGLA227 and ETH10. It can be assumed that the TGLA227 (77 bp) and ETH10 (209-211 bp) alleles among the SM cattle examined individuals were inherited from a B. indicus ancestor. On the other hand, the TGLA227 (89 bp) and ETH10 (217-219 bp) alleles were inherited from a B.taurus ancestor. Thus, the SM cattle presented with high level of taurine/zebuine admixture, which is consistent with the breeding history.
Acknowledgements
Financial support was received from the Ministry of Education and Science of Ukraine (state registration number 0117U000485) to Dr. Anna V. Lykhach and Dr. Alexander S. Kramarenko.
References
Adams, J. R., Leonard, J. A., & Waits, L. P. (2003). Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern US coyotes. Molecular Ecology, 12(2), 541-546. doi: 10.1046/j.1365-294X.2003.01708.x
Bicalho, H. M. S., Pimenta, C. G., Mendes, I. K. P., Pena, H. B., Queiroz, E. M., & Pena, S. D. J. (2006). Determination of ancestral proportions in synthetic bovine breeds using commonly employed microsatellite markers. Genetics and Molecular Research, 5(3), 432-437.
Bongso, T. A, Hilmi, M., Sopian, M., & Zulkilfi, S. (1988). Chromosomes of Gaur cross domestic cattle hybrids. Research in Veterinary Science, 44(2): 251 -254. doi: 10.1016/S0034-5288(18)30850-6
Bradley, D. G., MacHugh, D. E., Loftus, R. T., Sow, R. S., Hoste, C. H., & Cunningham, E. P. (1994). Zebu-taurine variation in Y chromosomal DNA: a sensitive assay for genetic introgression in West African trypanotolerant cattle populations. Animal Genetics, 25(S2), 7-12. doi: 10.1111/j.1365-2052.1994.tb00440.x
Chazara, O., Minvielle, F., Roux, D., Bed'hom, B., Feve, K., Coville, J. L., Kayang, B. B., Lumineau, S., Vignal, A., Boutin, J.-M., &
Rognon, X. (2010). Evidence for introgressive hybridization of wild common quail (Coturnix coturnix) by domesticated Japanese
quail (Coturnix japonica) in France. Conservation Genetics, 11(3), 1051 -1062. doi: 10.1007/s10592-009-9951 -8
Choroszy, B., Janik, A., Choroszy, Z., & Zabek, T. (2006). Polymorphism of selected microsatellite DNA sequences in Simmental
cattle chosen for identification of QTLs for meat traits. Animal Science Papers and Reports, 24(Suppl 2), 71 -77.
Cervini, M., Henrique-Silva, F., Mortari, N., & Matheucci Jr., E. (2006). Genetic variability of 10 microsatellite markers in the
characterization of Brazilian Nellore cattle (Bos indicus). Genetics and Molecular Biology, 29(3), 486-490. doi: 10.1590/S1415-
47572006000300015
Cosenza, M., Reale, S., Lupo, T., Vitale, F., & Caracappa, S. (2015). Allele frequencies of microsatellite loci for genetic characterization of a Sicilian bovine population. Genetics and Molecular Research, 14(1), 691-699. doi: 10.4238/2015.January.30.12
Czerneková, V., Kott, T., Dudková, G., Sztankóová, Z., & Soldát, J. (2006). Genetic diversity between seven Central European cattle breeds as revealed by microsatellite analysis. Czech Journal of Animal Science, 51, 1-7. doi: 10.17221/3902-CJAS Edwards, C. J., Gaillard, C., Bradley, D. G., & MacHugh, D. E. (2000). Y-specific microsatellite polymorphisms in a range of bovid species. Animal Genetics, 31(2), 127-130. doi: 10.1046/j.1365-2052.2000.00602.x
Egito, A. A., Paiva, S. R., Maria do Socorro, M., Mariante, A. S., Almeida, L. D., Castro, S. R., & Grattapaglia, D. (2007). Microsatellite based genetic diversity and relationships among ten Creole and commercial cattle breeds raised in Brazil. BMC genetics, 8(1), 83. doi: 10.1186/1471 -2156-8-83
Escobar, C. H., Ángel, M. O., Alfonso, H. O., & Guerra, M. T. (2009). Genetic variability of the zebu cattle breed (Bos indicus) in the departament of Huila, Colombia using microsatellite molecular markers. Acta Biológica Colombiana, 14(3), 173-180. Frantz, A. C., Zachos, F. E., Kirschning, J., Cellina, S., Bertouille, S., Mamuris, Z., Koutsogiannouli, E. A., & Burke, T. (2013). Genetic evidence for introgression between domestic pigs and wild boars (Sus scrofa) in Belgium and Luxembourg: a comparative approach with multiple marker systems. Biological Journal of the Linnean Society, 110(1), 104-115. doi: 10.1111/bij.12111
Frisch, J. E., Drinkwater, R., Harrison, B., & Johnson, S. (1997). Classification of the southern African sanga and East African shorthorn zebu. Animal Genetics, 28(2), 77-83. doi: 10.1111/j.1365-2052.1997.00088.x
Gómez, Y. M., Fernández, M., Rivera, D., Gómez, G., & Bernal, J. E. (2013). Genetic characterization of colombian Brahman
cattle using microsatellites markers. Russian journal of genetics, 49(7), 737-745. doi: 10.1134/S1022795413070041
Halbert, N. D., Ward, T. J., Schnabel, R. D., Taylor, J. F., & Derr, J. N. (2005). Conservation genomics: disequilibrium mapping of
domestic cattle chromosomal segments in North American bison populations. Molecular Ecology, 14(8), 2343-2362. doi:
10.1111/j.1365-294x.2005.02591.x
Hall, S. J., & Bradley, D. G. (1995). Conserving livestock breed biodiversity. Trends in ecology & evolution, 10(7), 267-270. doi: 10.1016/0169-5347(95)90005-5
Hammer, R., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4(1), 1-9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm Hanotte, O., Tawah, C. L., Bradley, D. G., Okomo, M., Verjee, Y., Ochieng, J., & Rege, J. E. O. (2000). Geographic distribution and frequency of a taurine Bos taurus and an indicine Bos indicus Y specific allele amongst sub-Saharan African cattle breeds. Molecular ecology, 9(4), 387-396. doi: 10.1046/j.1365-294x.2000.00858.x
Hartati, H., Utsunomiya, Y. T., Sonstegard, T. S., Garcia, J. F., Jakaria, J., & Muladno, M. (2015). Evidence of Bos javanicus * Bos indicus hybridization and major QTLs for birth weight in Indonesian Peranakan Ongole cattle. BMC genetics, 16(1), 75. doi: 10.1186/s12863-015-0229-5
Hussein, I. H. A. (2014). Phenotypic and Genotypic Characterization of Fuga Cattle of Western Sudan Compared to (Kenana and Butana) Dairy Breeds. Doctoral dissertation, University of Khartoum, Sudan.
Huxel, G. R. (1999). Rapid displacement of native species by invasive species: effect of hybridization. Biological Conservation, 89, 143-152. doi: 10.1016/S0006-3207(98)00153-0
Ibeagha-Awemu, E. M., Jann, O. C., Weimann, C., & Erhardt, G. (2004). Genetic diversity, introgression and relationships among West/Central African cattle breeds. Genetics Selection Evolution, 36(6), 673-690. doi: 10.1051/gse:2004024 Janík, A., Zabek, T., Radko, A., & Natonek, M. (2001). Evaluation of polymorphism at 11 microsatellite loci in Simmental cattle raised in Poland. Annals of Animal Science, 1(2), 19-29.
Janik, A., Zabek, T., & Radko, A. (2002). Identyfikacja polimorfizmu 11 loci mikrosatelitow u bydla rasy hereford. Medycyna Weterynaryjna, 58(11), 867-870 (In Polish).
Kesvulu, P. C., Rao, G. N., Niyazahmed, A. S., & Gupta, B. R. (2009). Molecular genetic characterization of Punganur cattle. Tamilnadu Journal of Veterinary and Animal Sciences, 5(5), 179-185.
Kharzinova, V. R., Dotsev, A. V., Kramarenko, A. S., Layshev, K. A., Romanenko, T. M., Solov'eva, A. D., Deniskova, T. E., Kostyunina, O. V., Brem, G., & Zinovieva, N. A. (2016). Study of the allele pool and the degree of genetic Introgression of semi-domesticated and wild populations of reindeer (Rangifer tarandus L., 1758) using microsatellites. Agricultural Biology, 51(6), 811 -823. doi: 10.15389/agrobiology.2016.6.811eng
Kundrat, R., Urban, T. (2007). Analyza variability mikrosatelitü u populací masnych plemen skotu v Ceské Republice/ In: VII-th International Conference of PhD. and MSc. Students "Genetics and Animal Breeding", May, 17-18, Brno, 22-29 (In Czech). Le Roux, J. J., Foxcroft, L. C., Herbst, M., & MacFadyen, S. (2015). Genetic analysis shows low levels of hybridization between African wildcats (Felis silvestris lybica) and domestic cats (F.s.catus) in South Africa. Ecology and Evolution, 5(2), 288-299. doi: 10.1002/ece3.1275
Lecis, R., Pierpaoli, M., Biro, Z. S., Szemethy, L., Ragni, B., Vercillo, F., & Randi, E. (2006). Bayesian analyses of admixture in wild and domestic cats (Felis silvestris) using linked microsatellite loci. Molecular Ecology, 15(1), 119-131. doi: 10.1111/j.1365-294X.2005.02812.x
Lirón, J. P., Peral-García, P., & Giovambattista, G. (2006). Genetic characterization of Argentine and Bolivian Creole cattle
breeds assessed through microsatellites. Journal of Heredity, 97(4), 331-339. doi: 10.1093/jhered/esl003
Loftus, R. T., Ertugrul, O., Harba, A. H., El-Barody, M. A. A., MacHugh, D. E., Park, S. D. E., & Bradley, D. G. (1999). A
microsatellite survey of cattle from a centre of origin: the Near East. Molecular Ecology, 8(12), 2015-2022. doi: 10.1046/j.1365-
294x.1999.00805.x
Luo, X. L., Song, H. F., & Guan, J. Q. (2014). Investigation on mechanism of sterility of male hybrids between yak and cattle. Journal of Applied Animal Research, 42(4), 395-399. doi: 10.1080/09712119.2013.875907
MacHugh, D. E., Shriver, M. D., Loftus, R. T., Cunningham, P., & Bradley, D. G. (1997). Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle. Genetics 146: 1071-1086.
MacHugh, D. E., Loftus, R. T., Cunningham, P., & Bradley, D. G. (1998). Genetic structure of seven European cattle breeds assessed using 20 microsatellite markers. Animal Genetics, 29(5), 333-340. doi: 10.1046/j.1365-2052.1998.295330.x Magee, D. A., Meghen, C., Harrison, S., Troy, C. S., Cymbron, T., Gaillard, C., Morrow, A., Maillard, J. C., & Bradley, D. G. (2002). A partial African ancestry for the Creole cattle populations of the Caribbean. Journal of Heredity, 93(6), 429-432. doi: 10.1093/jhered/93.6.429
Maudet, C., Luikart, G., & Taberlet, P. (2002). Genetic diversity and assignment tests among seven French cattle breeds based on microsatellite DNA analysis. Journal of Animal Science, 80(4), 942-950. doi: 10.2527/2002.804942x
Nijman, I. J., Bradley, D. G., Hanotte, O., Otsen, M., & Lenstra, J. A. (1999). Satellite DNA polymorphisms and AFLP correlate with
Bos indicus-taurus hybridization. Animal Genetics, 30(4), 265-273. doi: 10.1046/j.1365-2052.1999.00475.x
Nijman, I. J., Otsen, M., Verkaar, E. L. C., De Ruijter, C., Hanekamp, E., Ochieng, J. W., Shamshad, S., Rege, J. E. O., Hanotte, O.,
Barwegen, M. W., Sulawati, T. & Lenstra, J. A. (2003). Hybridization of banteng (Bos javanicus) and zebu (Bos indicus) revealed by
mitochondrial DNA, satellite DNA, AFLP and microsatellites. Heredity, 90(1), 10-16. doi: 10.1038/sj.hdy.6800174
Nikolov, I. S., Stoeckle, B. C., Markov, G., & Kuehn, R. (2017). Substantial hybridisation between wild boars (Sus scrofa scrofa)
and East Balkan pigs (Sus scrofa f. domestica) in natural environment as a result of semi-wild rearing in Bulgaria. Czech Journal
of Animal Science, 62(1), 1-8. doi: 10.17221/49/2015-CJAS
Novoa, M. A., & Usaquén, W. (2010). Population genetic analysis of the Brahman cattle (Bos indicus) in Colombia with microsatellite markers. Journal of Animal Breeding and Genetics, 127(2), 161-168. doi: 10.1111/j.1439-0388.2009.00811.x Nussberger, B., Greminger, M. P., Grossen, C., Keller, L. F., & Wandeler, P. (2013). Development of SNP markers identifying European wildcats, domestic cats, and their admixed progeny. Molecular Ecology Resources, 13(3), 447-460. doi: 10.1111/1755-0998.12075
Peakall, R., & Smouse, P. E. (2012). GenAIEx 6.5: genetic analysis in Excel. Population genetic software for teaching and researchd - an update. Bioinformatics, 28(19), 2537-2539. doi: 10.1093/bioinformatics/bts460
Pilarczyk, R., Vovk, S., & Kruzhel, B. (2015). Beef cattle breeding in Ukraine. Acta Scientiarum Polonorum. Zootechnica, 14(2), 322.
Polziehn, R. O., Strobeck, C., Sheraton, J., & Beech, R. (1995). Bovine mtDNA discovered in North American bison populations. Conservation Biology, 9(6), 1638-1638. doi: 10.1046/j.1523-1739.1995.09061638.x
Putnova, L., Vrtkova, I., Srubarova, P., & Stehlik, L. (2011). Utilization of a 17 microsatellites set for bovine traceability in Czech cattle populations. Iranian Journal of Applied Animal Science, 1(1), 31-37.
Qi, X. B., Jianlin, H., Wang, G., Rege, J. E. O., & Hanotte, O. (2010). Assessment of cattle genetic introgression into domestic yak populations using mitochondrial and microsatellite DNA markers. Animal Ggenetics, 41(3), 242-252. doi: 10.1111/j.1365-2052.2009.01989.x
Radko, A., Zyga, A., Zabek, T., & Stota, E. (2005). Genetic variability among Polish Red, Hereford and Holstein-Friesian cattle raised in Poland based on analysis of microsatellite DNA sequences. Journal of Applied Genetics, 46(1), 89-91. PMID: 15741669 Rhymer, J. M., & Simberloff, D. (1996). Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27(1), 83-109. doi: 10.1146/annurev.ecolsys.27.1.83
Rodriguez, D., Cedeno-Vazquez, J. R., Forstner, M. R., & Densmore, L. D. (2008). Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan Peninsula: II. Evidence from microsatellites. Journal of Experimental Zoology, 309A, 674686. doi: 10.1002/jez.499
Saturano, K. N., Herawati, E., & Setyawan, A. D. (2018). Interspecies and intraspecies genetic diversity of Ongole Grade cattle and Madura cattle based on microsatellite DNA markers. Biodiversitas, 19(4), 1593-1600. doi: 10.13057/biodiv/d190453 Sifuentes-Rincön, A. M., Puentes-Montiel, H., & Parra-Bracamonte, G. M. (2007). Assessment of genetic structure in Mexican Charolais herds using microsatellite markers. Electronic Journal of Biotechnology, 10(4), 492-499. doi: 10.4067/S0717-34582007000400002
Suprun, I. A., Ruban, S. Y., & Getya, A. A. (2016). Development status of meat cattle in Ukraine. Bulgarian Journal of Agricultural Science, 22(1), 140-142.
Stevanovic, J., Stanimirovic, Z., Dimitrijevic, V., Stojic, V., Fratrie, N., & Lazarevic, M. (2009). Microsatellite DNA polymorphism and its usefulness for pedigree verification in Simmental cattle from Serbia. Acta Veterinaria, 59(5-6), 621-631. doi: 10.2298/AVB0906621 S
Tumennasan, K., Tuya, T., Hotta, Y., Takase, H., Speed, R. M., & Chandley, A. C. (1997). Fertility investigations in the F1 hybrid and backcross progeny of cattle (Bos taurus) and yak (B. grunniens) in Mongolia. Cytogenetic and Genome Research, 78(1), 6973. doi: 10.1159/000134633
Verkaar, E. L., Nijman, I. J., Beeke, M., Hanekamp, E., & Lenstra, J. A. (2004). Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? Molecular Biology and Evolution, 21(7), 1165-1170. doi: 10.1093/molbev/msh064 Yoon, D. H., Kong, H. S., Oh, J. D., Lee, J. H., Cho, B. W., Kim, J. D., Jeon, K. J., Jo, C. Y., Jeon, G. J., & Lee, H. K. (2005). Establishment of an individual identification system based on microsatellite polymorphisms in Korean cattle (Hanwoo). Asian-Australasian Journal of Animal Sciences, 18(6), 762-766. doi: 10.5713/ajas.2005.762
Citation: Kramarenko, A.S., Karatieieva, O.I., Lykhach, A.V., Lugovoy, S.I., Lykhach, V.Ya., Pidpala, T.V., Patryeva, L.S., Kramarenko, S.S. (2019). Assessing genomic taurine/zebuine admixture in the southern meat cattle based on microsatellite markers. Ukrainian Journal of Ecology, 9(1), 251-261.
I (CI)E^^MI This work is licensed under a Creative Commons Attribution 4.0. License
