© The Authors, 2024, Published by the Universidad del Zulia*Corresponding author:clemus@uan.edu.mx
Keywords:
Genetic diversity
Landscape genetics
Native breeds
Genetic resources.
Exploring the genetic of three Hairless Pig breed populations in Mexico
Explorando la genética de tres poblaciones de la raza Cerdo Pelón en México
Explorando a genética de três populações da raça Porco Pelado no México
Gilberto Lemus Avalos
1
Javier Germán Rodríguez Carpena
2
William Orlando Burgos Paz
3
Clemente Lemus Flores
4*
Carlos Alfredo Carmona Gasca
4
Rev. Fac. Agron. (LUZ). 2024, 41(3): e244122
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v41.n3.02
Animal production
Associate editor: Dra. Rosa Razz
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
1
Doctorado en Ciencias Biológico Agropecuarias,
Universidad Autónoma de Nayarit. Doctorado en Ciencias
Biológico Agropecuarias en el Área de Ciencias Zootécnicas
y Veterinarias. Universidad Autónoma de Nayarit, Mexico.
2
Centro Nayarita de Innovación y Transferencia de la
Tecnología A.C. Tepic, Nayarit-México.
3
Corporación Colombiana de Investigación Agropecuaria-
AGROSAVIA. Centro de Investigación Turipaná, km 14 vía
Montería Cereté, Córdoba, Colombia.
4
Universidad Autónoma de Nayarit. Unidad Académica de
Medicina Veterinaria y Zootecnia. Compostela, Nayarit-
México.
Received: 17-05-2024
Accepted: 15-06-2024
Published: 01-07-2024
Abstact
The objective of this research was to carry out a molecular
genetic characterization of three Hairless Pig (HP) breed populations
located in México in the states of Nayarit, Oaxaca and Yucatán
to identify variations, selection eects and population genetic
relationships. From blood samples, a total of 163 animals from
three populations of HP were successfully genotyped. Genotyped
SNP data was employed to compute genetic diversity, population
structure and landscape genetic analysis. The parameters of
minor allele frequency (MAF), observed heterozygosity (Ho) and
Wright’s xation index (FIS) pointed out that the population of
Nayarit is the one with the greatest genetic diversity (MAF: 0.362,
Ho: 0.336, FIS: 0.061). Principal Component Analysis (PCA) and a
Neighbor-joining phylogenetic tree analysis showed diversication
among the three HP populations and pointed out a closer genetic
relationship between the HP populations and the Iberian pig breed.
The Admixture analysis showed as well common ancestry shared
from commercial and Iberian breeds in the HP populations in
dierent gradients. For the analysis of the relationships between
geographic and genetic distances, Mantel test was computed and the
results described a distribution pattern of the geographical locations
along the genetic distances similar to the clustering pattern of the
PCA and Neighbor-joining phylogenetic tree analysis. The results
obtained manage to present the HP poor conservation state and the
need to stablish a genetic conservation program meaning an eort
to prevent the loss of a signicant cultural, natural and genetic
resource.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2024, 41(3): e244122 July-September. ISSN 2477-9407.
2-6 |
Resumen
El objetivo de esta investigación fue realizar una caracterización
genética molecular de tres poblaciones de Cerdo Pelón (CP)
ubicadas en México en los estados de Nayarit, Oaxaca y Yucatán
para identicar variaciones, efectos de selección y relaciones
genéticas poblacionales. Se genotiparon con éxito un total de 163
animales de tres poblaciones de CP. Se emplearon datos de los
SNP genotipados para calcular la diversidad genética, la estructura
de la población y el análisis genético-espacial. Los parámetros de
frecuencia de alelo menor (MAF), heterocigosidad observada (Ho)
y el índice de jación de Wright (FIS) señalaron que la población
de Nayarit es la de mayor diversidad genética (MAF: 0.362, Ho:
0.336, FIS: 0.061). El Análisis de Componentes Principales (ACP)
y el análisis logenético mostraron una diversicación entre las tres
poblaciones de CP y señalaron una relación genética estrecha entre las
poblaciones de CP y la raza de cerdo ibérico. El análisis de Admixture
mostró también una ascendencia compartida de razas comerciales e
ibéricas en las poblaciones de CP. En el análisis genético-espacial los
resultados describieron un patrón de distribución de las ubicaciones
geográcas en relación con las distancias genéticas similar al patrón
de agrupamiento del ACP y del análisis del árbol logenético. Los
resultados obtenidos logran presentar el mal estado de conservación
del CP y la necesidad de establecer un programa de conservación
genética que signique un esfuerzo para evitar la pérdida de un
importante recurso cultural, natural y genético.
Palabras clave: diversidad genética, genética del paisaje, razas
nativas, recursos genéticos.
Resumo
O objetivo desta pesquisa foi realizar uma caracterização genética
molecular de três populações da raça Porco Pelón (PP) localizadas
no México nos estados de Nayarit, Oaxaca e Yucatán para identicar
variações, efeitos de seleção e relações genéticas populacionais. Um
total de 163 animais de três populações de PC foram genotipados
com sucesso a partir de amostras de sangue. Dados SNP genotipados
foram utilizados para calcular a diversidade genética, estrutura
populacional e análise genética da paisagem. Os parâmetros de
diversidade genética mostraram diferentes graus de diversidade entre
as três populações de PP e indicam que a população Nayarit é a que
apresenta maior diversidade genética. A Análise de Componentes
Principais (ACP) e a análise logenético de Neighbor-joining
mostraram diversicação entre as três populações de PP. A análise
de mistura mostrou uma ancestralidade comum compartilhada entre
raças comerciais e ibéricas (grupos externos) para populações de PP
em diferentes gradientes. Para analisar as relações entre distâncias
geográcas e genéticas, foi realizado o teste de Mantel e os resultados
descreveram um padrão de distribuição de localizações geográcas
em relação às distâncias genéticas semelhante ao observado no
padrão de agrupamento ACP e na análise logenético de Neighbour-
joining. Os resultados obtidos conseguem apresentar o mau estado de
conservação do PP e a necessidade de estabelecer um programa de
conservação genética que signique um esforço para evitar a perda
de um importante recurso cultural, natural e genético.
Palavras-chave: diversidade genética, genética da paisagem, raças
nativas, recursos genéticos.
Introduction
The introduction and presence of the pig in the country date
back 500 years ago and there are currently local genotypes whose
populations are in critical and risky conservation states, as is the case
of the Hairless Pig breed (DAD- IS, 2020; Sierra et al., 2016). The
Hairless Pig breed (HP) can be found in the tropical areas of Mexico
and its coasts, both the Gulf and the Pacic and center of the country as
well, adapted to dierent climates and altitudes in dierent production
systems (Lemus-Flores et al., 2001), the latter inuencing its genetic
composition and therefore its relevance in knowing them. Its physical
and morphological characteristics include visible “Iberian type”
features such as its grayish black color, rectilinear head, ears that fall
over the eyes, and the absence of hair (DAD-IS, 2020; Lemus-Flores et
al., 2020). For decades, the HP breed has had relevance in the survival
economy of the Mayan people and for this reason it is considered a
notable zoogenetic resource as it has great rusticity and the ability
to take advantage of foods with low nutritional content eectively,
in addition to being part in its traditional gastronomy (Hernández et
al., 2020; Rosado-Aguilar et al., 2022). The HP breed in Mexico has
been displaced from traditional production systems, thus decreasing
its populations due to the introduction of select breeds (Sierra et al.,
2005). At present, there is no formal record of an estimated number
of individuals along the country and in the ocial information
of this organism there is no phenotypic, productive or molecular
characterization data (DAD-IS, 2020). Despite the above, currently
there are eorts to rescue it since the demand for the consumption of
its products has increased, especially in the so-called gourmet market
(Hernández et al., 2020). By implementing current methodologies, it
is possible to determine the origin, genetic diversity, ancestry of the
HP breed and thereby implement strategies to know its current identity
and its genetic dierences with respect to other breeds to establish a
racial guarantee for both the breed and its products (Govindarajan
et al., 2012; Kawęcka et al., 2016). This research allowed, through
studies of SNPs in dierent populations of HP breed, to carry out a
study of genetic diversity and population structure that will allow us
to have a historical basis for future actions of genetic assessments in
support of rescue and conservation programs.
Material and methods
Sample collection, genotyping and quality control
This study was carried out in three populations of Hairless Pig
breed (HP) dened according to the characteristics described in the
study by Lemus-Flores et al. (2020) (absence of hair, black skin,
without spots, black hoof and straight snout) located in Mexico: the
northwest Pacic coast (Nayarit; 8 females and 2 males from the
Faculty of Veterinary Medicine and Zootechnics of the Autonomous
University from Nayarit, Compostela, semi-technied production
system), the southwest Pacic coast (Oaxaca; 8 females and 2 males
from the locality of San Francisco Ixhuatán, rustic production system)
and southeast Atlantic coast (Yucatán; 117 females and 26 males from
the Mexican Association of Iberian Origin Pig Breeders of Yucatán,
Tizimín, semi-technied production system) (gure 1). Unrelated
individuals were selected for this study.
Blood samples were taken from the jugular vein and collected in
Vacutainer EDTA K2 tubes (Becton Dickinson, Franklin Lakes, NJ,
USA) following the recommendations of the Ocial Standards NOM-
051-ZOO-1995 on the humane treatment of animals, and NOM-062-
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Lemus et al. Rev. Fac. Agron. (LUZ). 2024 41(3): e244122
3-6 |
ZOO-1999 on the technical specications for the production, care
and processing. Later, a blood sample from each tube was collected
individually in blood cards (Neogen, Nebraska, USA) and were
shipped to Neogen (Neogen, Nebraska, USA) for genotyping using
the Porcine GGP 50K microarray chip (Neogen, Nebraska, USA)
was used for genotype analysis. A total of 163 animals from three
populations of HP breed were successfully genotyped and a total of
46,145 autosomal SNPs, out of the 50698 SNPs. The quality control
of data obtained from the analyzes was carried out using the PLINK
v1.9 software (Chang
et al., 2015) where SNPs with polymorphisms
with a value > 0.90 were included and considering the MAF (minor
allele frequency) to a value < 0.01 were excluded.
Figure 1. Geographic locations of the three populations of Hairless
Pig described in the present study. NAY, Faculty of
Veterinary Medicine and Zootechnics of the Autonomous
University of Nayarit, Compostela, Nayarit (21°13’49”N
104°52’56”W); OAX, San Francisco Ixhuatán, Oaxaca
(16°20’57”N 94°28’57”W); YUC, Tizimín, Yucatán
(21°08’43”N 88°08’58”W).
Genetic diversity indices
The genetic diversity analysis was evaluated considering the
parameters of minor allele frequency (MAF), observed heterozygosity
(Ho), expected heterozygosity (He) and the xation index of
individuals within the populations (Fis) with the PLINK v1 software.
1.9 (Chang
et al., 2015).
Genetic structure and ancestry
Principal Component Analysis (PCA) and the construction of the
graphs were designed using the R software (R Core Team, 2021) to
establish sample clustering projection onto the axis using the three HP
breed populations (Nayarit, Oaxaca and Yucatán). In addition, publicy
SNP databases from Iberian, Duroc and Large-White breeds (Burgos-
Paz et al., 2013; Yang et al., 2017) were considered for comparisons.
Also, a Neighbor-joining phylogenetic tree was built with the
DarWin software (Perrier and Jacquemoud-Collet, 2006) based on
data on the genetic IBS (identity by state) distances between the
studied populations. A bayesian clustering of individuals was also
estimated using Admixture 1.3 (Alexander et al., 2009). Herein, the
K=1 to K=6 genetic groups (clusters) were tested and cross validation
error was used to select the most likely K according to the author.
Relationships between geographic and genetic distances
To determine the relationship between the geographic and genetic
distances of the HP breed populations, the Mantel test was performed
employing the GenAlEx 6.5 software (Peakall and Smouse, 2012)
using the site coordinates of the populations and the genetic IBS
distance matrix generated using PLINK v1 software 1.9 (Chang
et al.,
2015).
Results and discussion
Genetic diversity
The highest values of Minor Allele Frequency (MAF) were
observed for HP populations from Nayarit and Oaxaca, while that the
lowest were presented by the population of Yucatán. The values of
expected heterozygosity (He) were the same for the three populations,
while those of observed heterozygosity (Ho) were higher in the
Nayarit and Yucatán populations and lower in the Oaxaca population.
The highest values for the Inbreeding Coecient (FIS) were shown
by Oaxaca population, while in contrast, the lowest were presented
by the Yucatán and Nayarit populations. Similar diversity values
were registered in Muñoz et al. (2019) and Bordonaro et al. (2023) in
European local pig breeds where the average Ho, and He values were
from 0.270 to 0.297 and 0.275 to 0.303 respectively. The above seems
to indicate that the Nayarit population is the one with the greatest
genetic diversity, since it presents higher levels of He and Ho, followed
by the Yucatán and Oaxaca populations, presumably due to the lack of
adequate management of its crossing with other commercial breeds
(Meuwissen et al., 2020; DeWoody et al., 2021). The high FIS values
along with the low heterocigocity values (He, Ho) in the Oaxaca
population, suggested a considerable degree of inbreeding, since FIS
measures how much excess or reduction in heterozygosity is present
between observed and expected heterozygosities in a population (Li
et al., 2004). The above may be caused by the small number of the
population, the rustic production system from which they come and
the issues that it implies like poor breeding control (Šalamon et al.,
2019, Zhong et al., 2023).
Table1. Genetic diversity parameters of the three populations of
Hairless Pig described in the present study.
Population N MAF Ho He FIS
Nayarit
10 0.362 0.336 0.358 0.061
Oaxaca
10 0.312 0.302 0.358 0.160
Yucatán
143 0.263 0.332 0.358 0.072
N: Sample size, MAF: minor allele frequency, Ho: observed heterozygosity,
He: expected heterozygosity, FIS: Wright’s xation index, for each analyzed
population.
Genetic structure and ancestry
The grouping pattern observed in the PCA (gure 2) showed
three separated clusters for the HP breed populations and another
two individual clusters for the commercial breeds (Duroc and Large-
White breeds) except for the Iberian breed, which overlapped with the
Oaxaca HP breed population.
Also, a Neighbor-joining phylogenetic tree (gure 3) showed a
close relationship for the Yucatán and Oaxaca HP breed populations
are closer to the Iberian pig.
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Rev. Fac. Agron. (LUZ). 2024, 41(3): e244122 July-September. ISSN 2477-9407.
4-6 |
Figure 2. Principal Component Analysis employing genetic
distances and commercial pig breeds data. NAY:
Nayarit Hairless Pig breed population, OAX: Oaxaca
Hairless Pig breed population, YUC: Yucatán Hairless
Pig breed population, DUR: Duroc breed pig population,
LW: Large-White pig breed population, ESIB: Iberian pig
breed population.
This suggests a closer relationship between the Iberian breed with
the population of Nayarit compared to commercial breeds (Large-
White and Duroc breeds). The latter results along with the PCA
data analysis, shows a similar distribution pattern in the HP breed
populations. The dierent distribution of the genetic relationships
among the commercial breeds and the HP breed populations observed
in a dierent gradient, denote their genetic diversity possibly due
to the highly variable feeding and breeding practices that can be
found in native breed populations (Monteiro et al., 2019), as shown
in Šalamon et al. (2019) and Zorc et al. (2022) where the genetic
diversity of Croatian, Serbian and Eslovenian local pig breeds results
heterogeneous.
According to the results of the Admixture analysis (gure 4)
ancestry by the commercial breeds can be observed in the three HP breed
populations. We evaluated dierent K values with the mixed ancestry
model (K = 1 to 6) and the one with lowest CV value was chosen.
Greater ancestry was shown especially in the Nayarit population,
in contrast with the Yucatán population. It can be observed that the
patterns in the HP breed populations exhibit historical inuence of the
Iberian pig breed than to the other commercial breeds data (Duroc and
Large-White), especially the Oaxaca HP breed population, agreeing
with the above PCA and Neighbor-joining phylogenetic tree analysis
results, the latter, in accordance with Lemus et al. (2023), where they
founded closer genetic relationships between Iberian breeds and the
HP breed.
To determine the relation between geographical and genetic
distances of the HP breed populations, Mantel tests were performed
in GenAlEx 6.5 software (Peakall and Smouse, 2012) employing
the populations site coordinates and IBS (Identity by state) genetic
distance matrix (gure 5). The coecient of determination (r
2
)
was 0.63, suggesting a positive correlation between genetic and
geographical distances.
Figure 3. Neighbor-joining phylogenetic tree in root like pattern
employing IBS analysis data. NAY: Nayarit Hairless
Pig breed population, OAX: Oaxaca Hairless Pig breed
population, YUC: Yucatán Hairless Pig breed population,
DUR: Duroc breed pig population, LW: Large-White breed
pig population, ESIB: Iberian pig population.
Figure 4. The proportion of mixed ancestry in the populations
analyzed was evaluated by ADMIXTURE 1.3
(Alexander et al., 2009) with a K=3 value. We evaluated
dierent K values with the mixed ancestry model (K =
1 to 6). NAY: Nayarit Hairless Pig breed population, OAX:
Oaxaca Hairless Pig breed population, YUC: Yucatán
Hairless Pig breed population, DUR: Duroc breed pig
population, LW: Large-White breed pig population, ESIB:
Iberian pig population.
Throught the PCA, Neighbor-joining phylogenetic tree analysis
and Mantel test results, a pattern can be described in the relationship
between genetic dierentiation and geographical distances among the
three HP breed populations.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Lemus et al. Rev. Fac. Agron. (LUZ). 2024 41(3): e244122
5-6 |
Figure 5. Mantel test results. A distribution pattern can
be observed according to genetic distances and
geographical distances between populations.
The pattern showed greater diversity and dierentiation as the
spatial distribution of the three HP breed populations analyzed were
further from the southeast of the country (Yucatán) and its southwest
and northwest coasts (Oaxaca and Nayarit) (gure 1), drawing a gene
ow presumably carried out by anthropogenic factors, the latter,
possibly due to the original and rst introduction points of European
pig breeds in the colonization events of America during the 15
th
and
16
th
centuries carried out by the Spanish Empire (Hancock, 2022)
and clearly distinguishing three distinct groups, as it is analyzed
in Cesconeto et al. (2017) and Pimentel et al. (2023), where it is
established a positive correlation between geographical and genetic
distances in animals involved in anthropogenic activities (pigs
and horses respectively) clearly dierentiating them into dierent
regional groups.
The clear genetic diversity of HP populations throughout their
geographical distribution and how in dierent locations their genetic
structure continues to be dierent, indicates that even belonging
to the same race, the populations present great diversity between
them indicating that despite their state of conservation they present
levels of introgression by commercial breeds demonstrating a poor
conservation state and the need to stablish a genetic conservation
program.
Conclusions
The results obtained indicate that the three HP breed populations
analyzed in the present research are dierent from each other and the
genetic diversity analysis results suggest that they are closely related
to the Iberian breed, genetically distant from the commercial breeds
and, at the same time, share ancestry in dierent degrees with them.
The above seems to indicate that the genetics of the HP breed are
dierent according to its distribution throughout the country and their
heterogeneous production systems.
The latter unveils their poor conservation state and the need to
stablish a genetic conservation program, meaning an eort to prevent
the loss of a signicant cultural, natural and genetic resource.
Have a more detailed description of the current state of these
populations, manage to present a clearer perspective of the future
necessary actions that must be taken for their adequate conservation as
local breeds and, as far as possible, establish a genetic reserve program.
Acknowledgments
This study was supported and funded by the Secretary for
Research, Innovation, and Higher Education, Mérida, Yucatán,
Mexico. William Orlando Burgos Paz thank to Corporación
Colombiana de Investigación Agropecuaria – AGROSAVIA for the
support in data analysis (project ID 1002471).
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