INTRODUCTION

Since the arrival of pigs in America in the 16th century and their distribution throughout the new world, whether in natural or artificial selection, it has shaped the diversity of today’s populations. ^{Burgos-Paz et al. (2013)} described how the environment influenced the phenotypic differences between pigs in the highlands of Peru, in relation to those that inhabit lowland or tropical. Taking into account the wide range of climates in America, and particularly in the coasts, some pig populations are growing in size and relevance to human communities. This is the case of Yucatan hairless black pigs (YBH); this breed of pig has phenotypic peculiarities: black, hairless, flawless skin, black hoof and straight snout with an important participation in the food security of rural human populations (^{Lemus y Alonso, 2005}).

The FAO Animal Diversity Information System (^{DAD-IS, 2020}), considered that this breed was in danger of extinction, without a conservation program, and it is a valuable animal genetic resource that can contribute to food security in rural communities; as well as a reservoir of genetic diversity (^{Lemus-Flores et al., 2001}; ^{Scarpa et al., 2003}). In addition, the status of 38% of pig breeds worldwide is unknown (^{FAO, 2019}).

This hairless biotype comes from Iberian pigs (Sus mediterraneus), of African origin, introduced in all southern European regions (^{Benítez y Sánchez, 2001}). They were later introduced to America on Christopher Columbus’ second voyage in 1493 (^{Ogata, 2019}). YBH pigs are a genetic variation of Creole pigs (^{Su et al., 2014}) and are divided into two genetic lines; one located in populations in the Gulf of Mexico and the other population is present on the Mexican Pacific coast (^{Lemus-Flores et al., 2001}); it is called hairless Mexican, hairless or tropical hairless. They were at risk of extinction due to unplanned crossings with commercial lines of lean genotypes. Despite the fact that YBH is widely distributed on the Yucatan peninsula in Mexico, with low to medium-sized technical management. Currently, some pig farmers have found a valuable way to raise it, but the available information is limited in the population structure or lineage.

To obtain a breeding program in order, a large population of YBH was using a commercial SNP50K chip evaluated, to estimate the diversity and the actual population structure, as well as their genetic relationships for the future selection of feet of distant commercial breeds.

MATERIAL AND METHODS

RESULTS

Population structure

The first population structure was performed with a 10-fold cross-validation, to choose the best K value; the K=4 value presented the smallest cross-validation error (0.584). According to the mixture analysis, the YBH population is in three subpopulations structured (Table 1).

Table 1 Composition of the cluster predicted by ADMIXTURE (K4) 

	DUR	YUC1	YUC2	YUC3
DUR	0.99997	0.03532	0.00363	0.02726
YUC1	0.00001	0.69764	0.18677	0.18429
YUC2	0.00001	0.08993	0.64234	0.07703
YUC3	0.00001	0.17711	0.16726	0.71142

YUC1, YUC2 and YUC3 sub-populations of the hairless black pig of Yucatan. DUR Duroc breed population. The values per column of each breed indicate the proportions of other breeds.

With the ACP, YUC2 subpopulation is the most distant from the Duroc breed, with YUC1 and YUC3 closer because they share more Duroc genetic component (graph 1).

Graph 1 Analysis of the main components between subpopulations of hairless pigs and Duroc breed 

DISCUSSION

The 104 YBH samples chosen for the study were hairless muzzles, flawless black skin, black hull and straight foci to avoid phenotypic variations. The ADMIXTURE analysis subdivides them into three subpopulations. The introgression of the Duroc breed is very low in the three identified YBH subpopulations (YUC1, YUC2 and YUC3) from 0.00363 to 0.03532. It is similar to that of the Pampa Rocha pig from Uruguay (^{Montenegro et al., 2015}), inferior to the others Creole pigs in America, in which the Duroc component has an average of 0.15 and ranges from 0.00 (US Yucatan) to 0.45 (Moura Brasil) (^{Burgos-Paz et al., 2013}). The hairless pig in the Mexican Pacific has 0.20 of the Duroc component (^{Lemus et al., 2001}).

The separation of three subpopulations in the YBH and the low introgression of Duroc coincide with that observed by ^{Burgos-Paz et al. (2013)}. Modern pigs in the Americas are the result of many independent colonization events, but also to environmental challenges; as these YBH pigs are geographically isolated, far from commercial and hairless pigs, located on the Pacific and Gulf coasts. There is no evidence of an artificial breeding or breeding program with commercial breeds on the Yucatan peninsula.

There is a difference in genetic diversity between YBH subpopulations; in YUC3 it is taller, approaching random mating. It is likely that individuals from YUC1, YUC2 and Duroc show matings from individuals with greater genetic proximity in each subpopulation, which caused an increase in F and Fis. With the information generated, it is possible to program the mating in the subpopulations, generate more genetic diversity and avoid the request for variability, as occurs in Iberian populations (^{Esteve et al., 2013}). It is important to consider the statement by ^{Yang et al. (2017)}), indicating that populations with high Fis, normally present low diversity of haplotypes.

By identifying 93 SNPs that are different between populations of YBH vs Duroc, according to their extreme allele frequencies, higher frequency in Duroc and lower in YBN, we can use them as markers. According to ^{Yan et al. (2017)}, domestication and artificial selection, gave rise to a wide range of phenotypes among domestic pig breeds, which differ from their wild relatives; and that these are to behavior, body size, fertility, ability to move and adapt to food provided by humans related. Therefore, it is important to detect genetic loci, which may be involved in the transition from wild to domestic.

Considering that the American pigs are part of Iberian origin (^{Burgos-Paz et al., 2013}), YBH is phenotypically similar to the Iberian hairless, so that their coat is predominantly black and there are no white pigs. However, as ^{Ramírez et al. (2015)}, there were no SNPs related to the MC1R gene, which would allow considering the red or black color of the layer. Eight SNPs associated with epithelial cell differentiation, morphogenesis and epithelial development were identified; with five genes that could be studied as candidates for the hairless phenotype.

This study does not coincide with ^{Su et al. (2014)}, which proposes the BAMB1 gene as a strong hairless candidate; this gene was not different between the YBH and Duroc populations (p <0.35), with very similar allele frequencies. With ^{Burgos-Paz et al. (2013)} coincides with the PDE family genes, they report that in American Creole pigs the PDE10A and PDE11A genes are identified; the PDE8A gene is reported here. ^{Esteve et al. (2013)} in hairless Iberian pigs reports the FOXP1 gene as a candidate gene involved in the differentiation of epithelial cells, keratinization and the formation of hair follicles. In this study, the FOXA1 gene was identified, which is from the same family, also identified by ^{Yang et al. (2017}), which associates it with European pigs and relates it to the metabolism of proteins, glucose or fatty acids. For lipid metabolism ^{Esteve et al. (2013)}report eight candidate genes, not found in the PDHX, MFSD2A and ACSL1 report that were in this study identified; but for an immune response, these researchers coincide on the IL1RAPL2 gene, located on the X chromosome and IL6 on chromosome 7. On chromosome 6, the largest number of SNPs (27), involved in most biological functions, was identified. In this chromosome, for the transport of nutrients, ten SNPs were identified, for the MACF1 gene (cross-linking factor 1 of the microtubule-actin), identified in humans and mice as essential for embryonic development, to maintain the neuronal system and the integrity of the skin (^{Kang, et al., 2020}).

For muscle and skeletal development, the SNP BMP8B has been reported as an important gene for embryonic growth and development characteristics (^{Xiu-Kai et al., 2013}; ^{Ying et al., 2000}). For synapses and receptors, four genes related to brain and nervous disorders in humans have been identified what an opportunity for this pig to use it as a biomedical model. The GRM8 gene has also been reported by ^{Kwonm et al. (2019)} in Yucatan miniature pig, associated with nervous diseases in humans; similarly, the GABRA3 gene is associated with epileptic diseases (^{Niturad et al., 2017}), the SCL5A7 gene is associated with myasthenic congenital syndrome type 20 (Pardal-Fernández et al., 2018) and GRIK3 in neurophysiological processes.

The high number of SNPs identified as different between YBH and Duroc can be attributed to the lack of selection and crossing with the Duroc breed. Although further studies are needed to validate the role of the identified genes, these findings confirm that domestication and evolution are different between Duroc and YBH pigs.

CONCLUSION

In this first study with SNP50K in YBH pigs, the genetic difference of this pig is in comparison to the Duroc pig identified, providing useful genetic information for the conservation of this local genetic resource. YBH is far from Duroc, with a different population structure, genetic diversity and different genes involving important biological processes, which can be useful in the racial selection and differentiation program.

Suplementary information

Tabla A. List of 93 SNPs and genes associated with biological processes.