- Short communication
- Open Access
Introgression and isolation contributed to the development of Hungarian Mangalica pigs from a particular European ancient bloodline
© Marincs et al.; licensee BioMed Central Ltd. 2013
- Received: 29 November 2012
- Accepted: 15 June 2013
- Published: 1 July 2013
Mangalica breeds are indigenous to Hungary and their breeding history dates back to about 200–250 years ago. They are fat-type pigs and have a rare curly hair phenotype. The aim of our study was to establish the relationships between these unique breeds and other European breeds.
Based on a core sequence of 382 bp present in 2713 mitochondrial D-loop sequences from pigs belonging to 38 local breeds from nine countries, five cosmopolitan breeds and wild boars from 14 countries, we identified 164 haplotypes. More than half of the 2713 sequences belonged to either four haplotypes characteristic of continental European breeds or two haplotypes characteristic of British/cosmopolitan breeds; each haplotype is present in more than 100 individuals. Most Mangalica individuals belonged either to one of these common continental European haplotypes or to two Mangalica-specific haplotypes that were absent in all other breeds. In addition, we identified the ancestral mitochondrial D-loop signature present in these 2713 sequences and found that ~ 80% carried the European ancient signatures, ANC-Aside and ANC-Cside or their closely related signatures, while most of the remaining sequences carried a modern Asian signature, ANC-Easia. Mangalica individuals carried the ANC-Aside signature, but not the ANC-Cside or ANC-Easia signatures.
In all the Mangalica individuals, a unique ancient European signature was found in the mitochondrial DNA D-loop region, but they belonged almost exclusively to either certain very abundant European or two Mangalica-specific D-loop haplotypes. This indicates that the present-day Mangalica population in Hungary evolved either by introgression of other European breeds and wild boars or via total isolation after the divergence of European ancient porcine bloodlines.
- Wild Boar
- Wild Boar Population
- European Breed
- Curly Hair
- European Haplotype
There are hundreds of modern pig breeds and many of these are local breeds whereas only a few cosmopolitan breeds are used in the meat industry . The three Mangalica breeds, Blond, Red and Swallow-belly  are local, fat-type breeds with characteristic curly hair. They are farmed in Hungary, other successor states of the Austrian-Hungarian Empire and several other countries, and represent a niche pork market. The history of the Mangalica breeds dates back to the late 1700s when both spontaneous and conscious breeding started. Such breeding involved two old Mediterranean pig breeds, Sumadia and Syrmian that originated from the current territories of Serbia and Croatia, and three of the eight old pig breeds that were described in historical Hungary [3, 4] i.e. Bakonyi, Szalontai and Alföldi. To date, knowledge on the reproductive biology of the Mangalica breeds is quite extensive [5–9], while their genetics is less studied .
Although a number of studies have been conducted to examine the diversity, relationship and introgression between European pigs [11–16], Mangalica breeds have not been examined in this context. Here, we describe a large-scale comparative analysis of mitochondrial DNA (mtDNA) D-loop sequences of Mangalica and other European pig breeds in order to determine the molecular relationships between these breeds and their historical roots.
For this purpose, mtDNA D-loop sequences of 195 Mangalica individuals from a previous study  and 2518 additional sequences from the NCBI Genbank [see Additional file 1 and references therein] were combined. The collection covered wild boars from 14 countries, five cosmopolitan breeds, 38 local breeds from nine countries, and eight Mangalica pigs from an unspecified breed [see Additional file 1]. Haplotypes were determined using a 382 bp core sequence shared by all sequences [see Additional file 2]. Within this core sequence, 97 polymorphic positions were identified i.e. 52 transitions, 23 transversions, eight deletions, seven insertions and seven multiple variations, which resulted in 164 haplotypes [see Additional file 3].
Six major haplotypes, each one observed in more than 100 individuals, were identified i.e. HAP07, HAP08, HAP09, HAP13, HAP56 and HAP57. Haplotypes HAP07 and HAP08 correspond to the core European haplotypes C and A, respectively, as described previously [17, 18]. In terms of number of individuals, HAP08 was the most abundant haplotype (18.8%), followed by HAP09 (10.4%), HAP07 (9.1%), HAP13 (6.7%), HAP56 (5.6%) and HAP57 (4.3%) and each of these haplotypes was found in 33, 24, 27, 23, 15 and eight breeds and wild boar populations, respectively [see Additional file 4].
Among the 195 Mangalica individuals from our previous study , 56 belonged to the two major European haplotypes, HAP08 and HAP13, 91 to the Mangalica-specific haplotypes HAP15 and HAP16, 37 to haplotypes HAP44 and HAP45 and 11 to seven of the minor haplotypes. The eight Mangalica individuals without breed specification collected from another study [see Additional file 1] also belonged to haplotypes HAP08 and HAP13. Taking into consideration that Mangalica pigs separate into three breeds, i.e. Blond, Red and Swallow-belly, it is interesting to note that haplotypes HAP08, HAP15 and HAP45 were present in individuals of all three breeds, while no Red individual carried haplotypes HAP13 and HAP16, and no Swallow-belly individual carried HAP44. Red and Blond Mangalica breeds shared haplotype HAP44 with individuals from the Duroc, Large White and Tamworth breeds, and all three Mangalica breeds shared haplotype HAP45 with Austrian wild boars. Interestingly, the Mangalica breeds had no haplotype in common with the Hungarian wild boars. In this study, individuals associated with haplotypes HAP15 and HAP16 were found only in the Mangalica breeds. Thus, they probably represent Mangalica-specific maternal lineages.
Genetic distance values between pig breeds
BM vs. RM
BM vs. SM
RM vs. SM
Mean F ST 2
Mean Nei's distance 2
BM vs. non-M
0.52 ± 0.13
2.82 ± 2.21
SM vs. non-M
0.46 ± 0.15
2.34 ± 2.22
RM vs. non-M
0.33 ± 0.20
1.70 ± 2.45
non-M vs. non-M
0.33 ± 0.21
2.16 ± 2.48
An analysis on 208 European archaeological pig specimens identified five mtDNA D-loop signatures: ANC-Aside, ANC-Cside, ANC-Italy, ANC-Y1-6A and ANC-Y2-5A . Of these 208 samples, 109 (52.4%) carried ANC-Aside and 65 (31.25%) ANC-Cside, while the remaining 34 samples (16.35%) had one of the other three signatures. In a previous study, we showed that 197 (97%) of the 203 Mangalica individuals analysed (all included in the haplotype analysis described here) also carry the ANC-Aside signature, while the remaining six individuals carry signatures that are phylogenetically very close to ANC-Aside . To compare other European breeds with the Mangalica breeds and to determine the relationships to their ancestors, we identified the ancient signature of the remaining 2518 individuals of our current study and found that the ANC-Aside and ANC-Cside signatures were present in modern pigs at frequencies (42.5% and 33.5%, respectively) similar to those in the ancient pig specimens. In contrast, the frequency of the ANC-Italy, ANC-Y1-6A, and ANC-Y2-5A signatures dropped to less than 1.0% each. We note here that the ANC-Easia signature, which was not found in the European archaeological specimens , was observed in 455 of the 2713 modern pigs that we analysed. This is due, in part, to the introgression of Asian pig breeds into cosmopolitan and local British breeds, since 92.1% of the individuals with the ANC-Easia signature belong to these breeds.
Our analysis revealed that individuals that carried the major European haplotypes HAP07 or HAP09, HAP08 or HAP13 and HAP56 or HAP57 also carried ANC-Cside, ANC-Aside or ANC-Easia signatures, respectively [see Additional file 4]. It is important to note, that both the ANC-Aside and ANC-Cside signatures were present in several breeds and wild boar populations and consequently they can be characterised by more than one haplotype.
While Mangalica breeds can belong to several haplotypes, almost 50% of the breeds analyzed displayed only two haplotypes, HAP15 and HAP16, which were not present in any of the other breeds and wild boars studied. Furthermore, all 203 Mangalica individuals in this study carried the ANC-Aside signature.
Both the ANC-Aside and ANC-Cside signatures and the haplotypes HAP08 and HAP07 that carry them differ by one nucleotide substitution. Due to the difference between the lengths of the signature and the haplotype sequences [see Additional file 2], the calculated divergence time between ANC-Aside and ANC-Cside signatures, and between HAP08 and HAP07 is ~98 000 and ~190 000 YBP, respectively. This in good agreement with previously reported results [17, 20] and clearly indicates that the time of divergence between the European porcine maternal lineages carrying the ANC-Aside and ANC-Cside signatures is much older than the age of the oldest European archaeological specimen  and the predicted time of wild boar domestication .
In summary, we conclude that the present-day Mangalica population in Hungary may have originated by two different mechanisms: either introgression of common European bloodlines into the Mangalica breeds or by total isolation of some Mangalica ancestor species, as suggested by the presence of both common European and Mangalica-specific mtDNA D-loop haplotypes in the population.
The authors thank Drs Venkata S.R. Dukkipati and Zsolt Pénzes for their valuable comments and Professor Michael McManus for his critical reading of the manuscript. This work was supported by the Hungarian National Development Agency grant TECH_08-A3/2-2008-0405.
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