Monitoring of genetic diversity in Taiwan conserved chickensassessed by pedigree and molecular data Michèle Tixier-Boicharde, Chih-Feng Chena,f, Yen-Pai Leea a Department of Animal Scien
Trang 1Monitoring of genetic diversity in Taiwan conserved chickens
assessed by pedigree and molecular data
Michèle Tixier-Boicharde, Chih-Feng Chena,f, Yen-Pai Leea
a
Department of Animal Science, National Chung-Hsing University, Taichung 40227, Taiwan
b
Faculty of Animal Science, Vietnam National University of Agriculture, Trau Quy Town, Gia Lam District, Ha Noi City, VietNam
c
Key Laboratory of Animal Cell Technology, National Institute of Animal Sciences, Tu Liem, Hanoi, VietNam
d
Institut de Recherche pour le Développement, UMR Diversité, Adaptation et Développement des Plantes (DIADE), Avenue Agropolis, BP 64501, 34394
Montpellier Cedex 5, France
e
INRA/AgroParisTech, UMR1313 Génétique Animale et Biologie Intégrative, Jouy-en-Josas, France
f
Research Center for Integrative and Evolutionary Galliformes Genomics (iEGG), National Chung-Hsing University, Taichung 40227, Taiwan
a r t i c l e i n f o
Article history:
Received 9 August 2015
Received in revised form
27 December 2015
Accepted 29 December 2015
Keywords:
Conservation priorities
Effective population sizes
Inbreeding
Molecular data
Pedigree information
a b s t r a c t
Local chicken breeds face high risks of extinction A conservation program has been set up for eight Taiwan conserved chicken populations (TCP) The research presented here aims at estimating effective population size (Ne) and conservation priorities of TCP populations using pedigree and molecular data Genome diversity was assessed by genotyping 22 microsatellite markers in 45–50 animals per breed Results from the pedigree-based analysis showed that most Nevalues ranged between 50 and 100 except the Shek-Ki breed which exhibited the smallest value (46) so that most breeds could be considered as safe from a conservation point of view The change in inbreeding per generation varied between 0.7% to 1.9% depending on breeds Nevalues estimated from molecular-based analysis were generally lower than those estimated from pedigree-based analysis, suggesting a loss of diversity between the onset of the conservation program (from 1983 to 1995) and the start of pedigree recording in 2002 According to Ne
values, the TCP populations do not appear to be at a high risk, but mating plans by a rotation mating system should be designed in order to limit the increase in inbreeding Regarding the conservation strategy within the TCP, the Shek-Ki and Hua-Tung breeds showed the highest priority for conservation
in terms of genetic risk status and contributions to total diversity across pedigree- and molecular-based approaches In conclusion, this study of TCP populations shows how different types of data can be combined to define conservation priorities considering risk, diversity, or utility of local chicken breeds
& 2016 Published by Elsevier B.V
1 Introduction
Local chicken breeds play an important role in Taiwan due to the
traditional cuisine and culture Local chicken breeds may carry
disease-resistant genes and show high abilities to adapt to
alter-native farming systems, such as organic, which will particularly
improve animal welfare and food safety (Fanatico et al., 2009;Pham
et al., 2012) as well as adaptation to harsh environmental conditions
(Tixier-Boichard et al., 2009) Phenotypic data and pedigree
information have proven to be useful for characterization and management of genetic diversity (Boichard et al., 1997; Tixier-Boi-chard et al., 2009;Lenstra et al., 2012) Unfortunately, phenotypic data and pedigree records of local chickens are rarely documented
in reality (Tixier-Boichard et al., 2009) Therefore, molecular mar-kers are used to monitor the loss of genetic diversity of populations and set priorities for conservation (Boettcher et al., 2010)
FAO (2014)reported that 21.3 percent of chicken breeds in the world were classified as being at risk of extinction, highlighting the importance to assess genetic diversity and the current popu-lation status This percentage might be higher than that because of
a large number of populations with an unknown status in devel-oping countries Basically, there are three strategies for setting priorities in conservation such as the maximum-risk strategy, the maximum-diversity strategy as well as the maximum-utility strategy (Bennewitz et al., 2007)
The maximum-risk strategy is based on the numbers of
Contents lists available atScienceDirect
Livestock Science
http://dx.doi.org/10.1016/j.livsci.2015.12.013
1871-1413/& 2016 Published by Elsevier B.V.
n Corresponding author at: Faculty of Animal Science, Vietnam National
Uni-versity of Agriculture, Trau Quy Town, Gia Lam District, Ha Noi City, VietNam.
E-mail addresses: phammanhhung@vnua.edu.vn (M.-H Pham),
hoantranvcn@yahoo.com (X.-H Tran),
c.berthouly@gmail.com (C Berthouly-Salazar),
michele.boichard@jouy.inra.fr (M Tixier-Boichard),
cfchen@dragon.nchu.edu.tw (C.-F Chen), yplee@mail.nchu.edu.tw (Y.-P Lee).
Trang 2breeding animals (FAO, 2000), inbreeding rate (EAAP, 1998;
Meu-wissen, 2009) and recommended effective population size (Ne)
(Meuwissen, 2009) The Nemeasures the number of breeding
in-dividuals in an idealized population in equilibrium that would
show a similar trend in inbreeding as the population under study,
it is one of the most pivotal parameters in both evolutionary
biology and conservation of genetic diversity (Waples and Do,
2010; Goyache et al., 2011; Leroy et al., 2013) This parameter is
considered as one of the major criteria for monitoring risk status
in livestock populations because it accounts for inbreeding and
loss of genetic diversity through random genetic drift (Falconer
and Mackay, 1996;Meuwissen, 2009).Leroy et al (2013)showed
that estimates of effective population size varied according to the
within-breed genetic structure, for different species (i.e cattle,
dog, horse and sheep)
The maximum-diversity strategy defines that a breed is
se-lected for conservation when it contributes significantly to the
overall genetic diversity weighted by both the between- and
within-breed diversity Breeds can be ranked according to their
contribution either to the actual or to the predicted future
di-versity (Bennewitz et al., 2007) For instance,Zanetti et al (2010)
set up conservation priorities forfive Italian local chicken breeds
undergoing in situ conservation using 20 microsatellites In the
case of Vietnamese domestic chickens,Pham et al (2013a)showed
with the highest priorities for conservation according toCaballero
and Toro (2002), andPetit et al (1998) approaches, taking into
account within- and between-breeds components of diversity
When possible, pedigree information and molecular data
should be combined for decision making of conservation priorities
(Zanetti et al., 2010) Pedigree-based and molecular-based
esti-mates of genetic diversity may be more or less correlated
de-pending on the pedigree completeness and the number of markers
(Toro et al., 2006) as illustrated in Iberian pigs with correlations
between pedigree inbreeding and marker homozygosity ranging
from 0.69 with 49 microsatellites (Toro et al., 2002) to 0.92 with
60 K SNPs (Silió et al., 2010) Furthermore, perfect correlations
between approaches cannot be reached because pedigree-based
estimates do not take into account Mendelian sampling, and it is
known that full-sibs would share between 45% and 55% of their
genes rather than exactly 50% in a traditional relationship matrix
(VanRaden and Tooker, 2007) An additional difference between
pedigree- and molecular-based analyses is the definition of the
founder population, which depends on the depth of pedigree for
pedigree-based analysis, the more complete the pedigree, the
more ancient the founder population (Falconer and Mackay, 1996)
Consequently, pedigree- and molecular-based analysis is using
different information, as pedigree-based analysis reflects only
di-versity due to relatively recent ancestry, depending on the
popu-lation history (Toro et al., 2006;Engelsma et al., 2012)
The purposes of this study were (i) to assess genetic diversity
with pedigree-based estimates and molecular-based estimates for
eight populations kept under a conservation program in Taiwan
since 1982, and (ii) to monitor trends in genetic diversity and to
make recommendations for conservation strategy
2 Material and methods
2.1 Data
Conservation of native chickens in Taiwan started from 1982,
when native chickens were collected around the islands and
conserved at National Chung-Hsing University (NCHU)
experi-mental farm Eight Taiwan conserved chicken populations (TCP: B
strain, L2 strain, Hsin-Yi, Hua-Tung, Ju-Chi, Nagoya, Quemoy and
Shek-Ki) have been conserved at NCHU experimental farm since then (Lee, 2006) The L2 and B strains were selected by NCHU from
strains were closed populations since their establishment in 1983, while B strain was a male line and a L2 female line for crossing to produce commercial meat-type chicken Since then, they have been selected for 24 and 26 generations, respectively, and have been extensively used in research as well as in production (Chao and Lee, 2001; Chen et al., 2007; Pham et al., 2013b) A small
man-agement of conserved chicken populations followed a routine procedure (Chao and Lee, 2001) Chicks were raised infloor pens until 16 week of age, when they were transferred to individual wirefloored cages Artificial insemination was individually used for the female chickens with sire known and dam known On the average, the generation interval of TCP populations was one gen-eration per year (Table 2) For the present study, pedigree in-formation recorded between 2002 (starting with ancestors in 2001) and 2008 were used to estimate the effective population size with different methods The pedigree information included a total of 4283 individuals and the numbers of founders at the onset
of pedigree recording are shown inTable 2 In addition, samples from 383 individuals (i.e 288 individuals from six TCP born in
2003 and 95 individuals from B and L2 strains born in 2008) were genotyped and part of the data was previously published ( Ber-thouly et al., 2008;Chang et al., 2012;Pham et al., 2013b) Briefly,
an average of 48 individuals per population was genotyped for 22
Table 1 Pedigree information in the first generation of the eight populations when con-servation program started.
Population First generation
N es , effective population size based on number of sires and dams; and ΔF, rate of hypothetical inbreeding (in percentage) for a population with such an effective population size.
Table 2 Number of founders at the onset of pedigree recording and average number of male and female in the 2002–2008 periods for the eight populations.
Population Founders in 2001 2002–2008 generations
L2 strain 16 328 61.0 0.82 20.8 194.2 75.2 0.67 5
N es , effective population size based on number of founder animals; ΔF, rate of hypothetical inbreeding (in percentage) expected for a population with N es ; N m , average number of male; N f , average number of female; N es , effective population size based on number of breeding animals; and ΔF, rate of hypothetical inbreeding (in percentage) expected for a population with N es across the 2002–2008 genera-M.-H Pham et al / Livestock Science 184 (2016) 85–91
86
Trang 3samples were used to estimate the contemporary effective
popu-lation size and contributions to diversity
2.2 Demographic and Pedigree-based analysis
2.2.1 Effective number of founders
The effective number of founders (fe) is the number of equally
contributing founders, which would give the same amount of
genetic diversity that is present in the current population This
was calculated as inLacy (1989), and it is usually much smaller
than the actual number of founders in pedigree (animals with both
parents unknown) because of unequal contributions of founders to
the current population
2.2.2 Effective number of ancestors
The effective number of ancestors (fa) was calculated as in
Boichard et al (1997), explaining the complete genetic diversity of
a population When compared with the effective number of
founders, it provides evidence of bottlenecks that occurred in
population in the past
2.2.3 Effective number of founder genomes
The loss of genetic diversity would occur due to genetic drift in
a small population, even if founders would contribute equally to
this population (Ballou and Lacy, 1995) Therefore, the effective
number of founder genomes or founder genome equivalent (fge) is
defined as the number of equally contributing founders with no
loss of founder alleles that would give the same amount of genetic
diversity as is present in the reference population The fge was
calculated as inCaballero and Toro (2000) It accounts for the loss
of genetic diversity that occurred in the population due to genetic
drift and bottlenecks
2.2.4 Effective number of nonfounders
The effective number of nonfounders (Nenf) was calculated as
−
⎛
Nenf f1 f1 ,
1
nonfounders and for loss of genetic diversity due to drift
accu-mulated over nonfounder generations (Caballero and Toro, 2000)
2.2.5 Measure of the loss of genetic diversity
Measures of the loss of genetic diversity can be derived from fe,
fge, and Nenf The amount of genetic diversity (GD) in the reference
f
1
2ge When expressed as 1GD, it measures the genetic
diversity loss in the population since the founder generation, as a
f
1
2e
1GD*measures the loss of genetic diversity that occurred in the
population due to the unequal contributions of founders before
their contributions converged (Caballero and Toro, 2000) The
difference between GD*and GD isGD* −GD= 2N1
enf, which mea-sures the loss of diversity by genetic drift accumulated over
non-founder generations (Caballero and Toro, 2000)
2.2.6 Effective population size based on the mating plan
The estimation of effective population size based on number of
sires and dams (Nes) followsWright’s (1931)model This method
makes possible to predict Nesunder several assumptions,
includ-ing random matinclud-ing, absence of selection and random variation
of progeny size across parents (Leroy et al., 2013) Computation
+
N N
es
4m f
(ΔF) is inversely proportional to the number of Nes: ΔF =
N
1
2es
2.2.7 Effective population size based on individual inbreeding rate The effective population size based on the individual increase
in inbreeding (Nei) was computed for each population (Gutiérrez
et al., 2008) The individual increase in inbreeding is defined as
ΔFi= –1 gi 1− 1–Fi, where Fi is the inbreeding coefficient for each individual i, and giis the equivalent complete generations ( Gu-tiérrez et al., 2009) The mean of theΔFivalues computed for the n
individuals belonging to a given population of individuals (ΔF ) can
be used to estimate Neiby the method ofCervantes et al (2008)
Δ
N
F
ei 21 2.2.8 Effective population size based on individual coancestry rate The realised effective population size (Nec) was calculated for each population based on the individual increase in coancestry rates (Cervantes et al., 2011) The increase in coancestry between
( + )
gj gk
where cjkis the inbreeding of an offspring from j and k, and gjand
in-dividual j and k, respectively By averaging the increase in coan-cestry for all pairs of individuals in a reference subpopulation, we can estimate an effective population size based on coancestries as
= Δ
1
2 The confidence interval of the estimated values of Nei
and Neccan be computed using the variance ofΔFiandΔcjkfrom the individuals in each population (Gutiérrez et al., 2008) The genealogical information was analyzed using the program Endog v4.8, a computer program for monitoring genetic variability of populations using pedigree information (Gutiérrez and Goyache,
2005)
2.3 Degree of nonrandom mating
correlation of genes within individuals relative to the correlation
of genes taken at random from the population as inCaballero and Toro (2000) This coefficient gives an indication of the deviation from Hardy–Weinberg equilibrium expectations and it is related to inbreeding and coancestry coefficient by (1F)¼(1f) (1α), where F and f are the inbreeding and coancestry coefficients, re-spectively (Wright, 1969)
2.4 Molecular-based analysis 2.4.1 Microsatellites genotyping and polymorphism The presence of null alleles was tested using FreeNA software (Chapuis and Estoup, 2007) in which loci with estimated fre-quencies of null alleles above 0.2 are considered to be potentially problematic for calculations The null allele frequency estimated for the 22 loci was lower than 0.2 (data not shown) so we assumed that null alleles were absent and used for our analyses The matrix
of Nei's DAgenetic distances (Nei et al., 1983) was computed by Populations package 1.2.32 (Langella, 1999)
2.4.2 Contemporary effective population size Contemporary effective population size (NeLD) was computed from genotypic data by a point estimation method using linkage disequilibrium (Hill, 1981; Waples, 2006) This method was
cor-rects for biases resulting from the presence of a wide range of
Trang 4(2006) The NeLD could be calculated for unlinked loci
( × ( – ))
N
r
3
S
2 1 , where r is correlation among alleles and S is
sample size (Hill, 1981;Waples, 2006) All alleles with frequencies
less than the critical values (Pcrit) of 0.05 were excluded (Waples
and Do, 2008) A jackknife method was used to construct 95% CIs
of the estimates
2.5 Contributions to diversity
The contribution of each breed to total genetic diversity was
computed by three approaches: a method based on molecular
coancestry (Caballero and Toro, 2002), a method based on allelic
richness (Petit et al., 1998) and a Weitzman approach modified by
Ollivier and Foulley (2005)
The method described byCaballero and Toro (2002)uses as a
criterion for the maintenance of the maximum overallNei’s (1987)
gene diversity (GD) minimizing the average of molecular kinship
within subpopulations (fs), the average of molecular coancestry
genetic distance between subpopulations (Nei, 1987) Total gene
diversity (GDT) is GDT¼1fm Genetic diversity within
sub-populations is GDW¼1fs Genetic diversity between
subpopula-tions is GDB¼fsfm This approach estimates the genetic diversity
remaining when removing a breed Therefore, a positive value will
indicate that higher diversity is obtained when a breed is not
in-cluded in the dataset
The method described byPetit et al (1998), is using the rarefied
number of alleles per locus, and was applied to assess the
con-tribution of each subpopulation to total allelic richness (CT) in
meta-population The CTincluded the AR of within-subpopulation
diversity (CS) and its divergence from other subpopulations (CD)
and therefore taking into account private alleles In contrast to the
method of Caballero and Toro, this one estimates a contribution to
genetic diversity Therefore, positive value would indicate that
when population is included into the dataset it would increase
genetic diversity Contributions of the breeds to diversity were
computed using Molkin 3.0, a computer program for genetic
analysis of populations using molecular coancestry information
(Gutiérrez et al., 2005)
The method described by Ollivier and Foulley (2005),
con-tributions to between-breeds diversity (CB) were assessed by
using marginal loss of genetic diversity, based on DAgenetic
dis-tances (Nei et al., 1983), following Weitzman approach (Weitzman,
1993) implemented in WEITZPRO (Derban et al., 2002)
Within-breed contributions to diversity (CW) and aggregate diversity (D)
were calculated as suggested byOllivier and Foulley (2005) The D
index was obtained after weighting CB by FSTand CW by 1FSTas
the following formula: D¼FST CBþ(1FST) CW
3 Results and discussion 3.1 Pedigree-based analysis 3.1.1 Inbreeding and effective population size The estimates of hypothetical inbreeding increment per gen-eration are given in Table 2 The highest ΔF was approximately 1.3% found in Shek-Ki and B strain that means that in average 1.3%
of heterozygosity was lost per generation.Table 3showed that the highest increase in inbreeding rates was found for Ju-Chi, Hua-Tung and Shek-Ki populations at the values of 1.34%, 1.76% and 1.88%, respectively, which exceeded the maximum level of one
Additional management such as mating decisions (avoidance of mating between relatives by forming 20 mating pairs) and opti-mum contribution selection (Grundy et al., 1998) should be con-sidered Avoiding mating between close relatives can be easily
mated to a group of sisters/half-sisters, and the son of this male‘X’ will be mated to the daughters of another male‘Y’ which has no
coancestry coefficients and to design the mating plan in a way to minimize the average coancestry of parents by the software Fa-mily sizes should be kept homogenous, with always one son kept per sire family and at least one daughter kept per dam An increase
of generation interval for these breeds could also minimize in-breeding and thus a better conservation of their genetic diversity The estimation of Nevalues highly varied between breeds and
ranged from 38.3 in Shek-Ki to 75.2 in L2 strain, and were always lower than those estimated for 2001, except for B and L2 strains (Table 2) All but the Shek-Ki breed (Nei: 45.9) showed Neivalues within the recommended minimum levels between 50 and 100 to maintain genetic variation for a population in a long term ac-cording toMeuwissen (2009) The average coancestry rates, cor-responding to the expected inbreeding rates in the next genera-tion, varied from 0.77 in L2 strain to 3.14% in Shek-Ki (Table 3) The
Necvalues were approximately equal to one-third of the Neivalues,
as indicated by the Nec/Neiratio, and ranged from 21.0 in Shek-Ki to 35.9 in L2 strain (Table 3;Fig 1) The ratio between Nec and Nei
values was lower than one, which reflected that no substructure (Wahlund effect) is found within eight populations (Cervantes
et al., 2011)
Correlations between Nesand other Nemeasures (Nei, Nec) were positive but not significant (Spearman's rank correlation¼0.51, Table 3
Estimates of effective population sizes for each population obtained by the pedigree and molecular data.
Population Pedigree information a
Linkage disequilibrium b
N
ec ei
an, number of individuals; ΔF , the rates of inbreeding per generation (in percentage); Nei, effective population size based on individual increase in breeding; Δc, the rates
of coancestry per generation (in percentage); N ec , effective population size based on increase in coancestry; and ratioN
N
ec
ei
b
M.-H Pham et al / Livestock Science 184 (2016) 85–91 88
Trang 50.57, P40.05).
3.1.2 Genetic contributions
For the period between 2002 and 2008, the estimated values of
the fe, fa, fge, Nenfand Na50in eight populations are given inTable 4
They were always higher than the real number of founders
re-corded in the early generations between 1983 and 1995 In
Shek-Ki, the estimated values were consistently lower than in the
re-maining seven populations, except for Nenf, which was lower in
Hua-Tung The fe, faand fgevalues for Shek-Ki were 21, 20 and 16,
respectively The numbers of ancestors needed to explain 50% of
the gene pool ranged from 7 in Shek-Ki to 16 in L2 strain These
results indicate that Shek-Ki has a narrow genetic base and
con-tributes less to the within-breed component of genetic diversity
than the remaining populations The effective number of
non-founders was greatly higher than effective number of founder
genomes, which indicates that loss of genetic diversity due to drift
was accumulated over nonfounder generations
The loss of overall genetic diversity observed in Hua-Tung and
Shek-Ki was 5.2% and 6.3%, respectively Thefirst loss ranged from
2.6% in Hua-Tung to 3.1% in Shek-Ki due to bottlenecks and genetic
drift (Fig 2) The second loss accounted for unequal founder
contribution and ranged from 1.7% in Hua-Tung to 2.4% in Shek-Ki
The remaining loss was due to genetic drift only
3.2 Degree of nonrandom mating
The average inbreeding coefficients were smaller than average
coancestries in all eight populations (Table 4) Therefore, the de-gree of nonrandom mating has been negative and mating of highly average-related individuals was successfully avoided The average inbreeding rates were moderate and ranged from 2.1% in Nagoya
to 7.2% in Shek-Ki for the last generation (Table 4) However, these values do not take into account the fact that the founders in 2001 could have been already inbred because each population was closed since several generations In practice, chickens showing a low individual inbreeding should be chosen for mating in order to maintain the recommended effective population sizes and to prevent the risk of extinction in small populations
3.3 Molecular-based analysis 3.3.1 Contemporary effective population size The estimates of NeLDwere lower than the ones of Neigiven by the pedigree-based analysis and that of Nesvalues (Tables 2and3; Fig 1) The correlations between NeLD and Nes was very low (Spearman’s rank correlation¼0.24); but it was significantly
correlation¼0.85, 0.83 and 0.83, respectively, Po0.05) The sam-ple size used for genotyping was included in the CIs of NeLD It is possible that this underestimation is due to the small number of molecular markers used (Waples, 2006; Engelsma et al., 2012) Engelsma et al (2010)showed that marker density was important
in order to assess genetic diversity with heterozygosity estimates but was not so much important when an IBD method was used to assess diversity
The difference between molecular-based estimate of Ne and pedigree-based estimates of Necould also occur if a loss of di-versity took place between the initial founder generation and the first generation included in the pedigree Pedigree-based esti-mates are as good as the pedigree data, which, in the present case, represents a quite recent part of the history of populations Ac-cording toToro et al (2006), some important loci might be highly differentiated because selective forces are strong enough at such loci to overcome the effect of low effective size In order to maintain genetic diversity in a gene bank of Holstein cattle, En-gelsma et al (2012) concluded that high density SNP-based di-versity provided a more detailed knowledge of didi-versity at the scale of chromosomal regions than pedigree-based estimate of diversity, which remains global
3.3.2 Contributions to diversity The conservation priorities were mostly consistent across three approaches we used Contribution to global diversity (GDG) was significantly negatively correlated with total allelic diversity (CT, Spearman’s rank correlation¼ 0.83, Po0.05) and with aggregate diversity (D, Spearman's rank correlation¼ 0.93, Po0.001) The
Fig 1 Effective population sizes for each population obtained by the pedigree and
molecular data N ei , effective population size based on individual increase in
breeding with its standard error bars; N ec , effective population size based on
in-crease in coancestry with its standard error bars; and N eLD , contemporary effective
population size for each population.
Table 4
Genetic contributions of eight Taiwan conserved chicken populations.
Population n f e f a f ge N enf N a50 F f F 2008 7SE
B strain 595 44 21 31.6 112.1 8 0.011 0.017 0.05170.006
L2 strain 1346 87 45 65.5 265.0 16 0.006 0.007 0.02570.003
Hsin-Yi 362 41 38 31.1 128.8 14 0.010 0.017 0.04870.015
Hua-Tung 386 29 27 19.3 57.7 10 0.019 0.026 0.06570.011
Ju-Chi 424 28 27 20.3 73.8 10 0.013 0.025 0.03870.004
Nagoya 428 38 31 30.1 144.8 11 0.008 0.018 0.02170.003
Quemoy 419 31 26 22.8 86.2 10 0.009 0.022 0.03570.004
Shek-Ki 323 21 20 16.0 67.2 7 0.020 0.031 0.07270.013
n, number of individuals; f e , estimates of effective number of founders; f a , effective
number of ancestors; f ge , effective number of founder genomes; N enf , effective
number of nonfounders; N a50 , number of ancestors explaining 50% of the gene
pool; F, inbreeding coefficient for each population in the 2002–2008 periods; f,
coancestry coefficient for each population in the 2002–2008 periods; and F 2008 ,
inbreeding coefficient of the last generation in 2008; SE, standard error.
Fig 2 Genetic diversity (GD) loss in eight populations in the period between 2002 and 2008 GD loss due to bottlenecks and genetic drift (1GD); due to unequal founder contribution (1 GD *
); and genetic drift only (GD * GD).
Trang 6D index was positively correlated with the CT (Spearman's rank
correlation¼0.91, Po0.01) Negative correlation is expected with
GDGsince it expresses a loss why other methods express a gain
The results showed that Shek-Ki had the highest contributions
(GDG¼ 2.47%, CT¼5.33% and D¼8.29%) to overall genetic
di-versity (Table 5) Nagoya ranked the second contributions to
di-versity (GDG¼ 1.76% and D¼7.02%), and the fourth of CT¼2.73%
GDWfor conservation, whereas the traditional Ju-Chi breed had
the smallest values of diversity (GDG¼1.21%, CT¼ 1.64% and
D¼ 0.47%) for conservation priorities Overall, the Shek-Ki,
Hua-Tung and Nagoya had high conservation priorities in terms of
genetic diversity However, Shek-Ki and Nagoya exhibited very low
within-breed diversity and it was highly differentiated from other
breeds and appeared as obvious conservation priorities When
analysed for six TCP (i.e not including B and L2 strains), the
Hua-Tung contributed the highest to the aggregate diversity (Berthouly
et al., 2008) Thus, using a different set of breeds seems to change
the relative contribution of each breed, as observed in 24
Vietna-mese domestic chicken populations (Pham et al., 2013a) In fact,
the main contribution of the Hua-Tung was based on its gene
di-versity and thus this breed had a high contribution to the gene
pool
3.4 Potential conservation
We have analyzed genetic diversity for eight Taiwan conserved
chicken breeds based on both pedigree and molecular data The
smallest values of effective population size based on pedigree
in-formation were observed in Shek-Ki and Hua-Tung breeds Thus,
the Shek-Ki and Hua-Tung breeds showed high priorities for
conservation in terms of genetic risk status and contributions to
diversity In spite of a very small number of founders in thefirst
generation, the Hua-Tung breed exhibited the highest contribution
to within-breed diversity It is likely that the initial founders were
very diverse because of the breed history: farmers kept this breed
together with others in the backyard, so that Hua-Tung might have
been crossed with imported larger game birds from Southeast Asia
(Lee, 2006;Berthouly et al., 2008), which have bright black feather
and large body size Quemoy exhibited also a relatively high NeLD
and Neiin spite of a very narrow base population Contrasting with
the history of the Hua-Tung breed, the Quemoy breed is expected
to be a true native since it was essentially isolated from outside the
world between 1949 and around 1990 Although chickens were
also kept in the backyard, the original owners intentionally kept
them as pure as possible (Chia-Juing Won, personal
communica-tion) However, the Quemoy conservation program is the most
recent of all populations, since it started in 1995 Thus, it is likely
that effects of genetic drift have been less important in this breed than in others Therefore, the effective numbers of founder gen-omes of Hua-Tung and Quemoy showed high values, for different reasons
Considering the maximum-utility approach is also needed be-fore making recommendations for conservation Conservation priorities should include the market demand, survivability and productivity related to specific genes under existing management conditions, scocio-economics and the needs for research and de-velopment (Toro et al., 2006;Pham et al., 2013a) In this respect, Shek-Ki has been selected as a sire line to be distributed to farmers producing the Three Yellow breed for meat consumption in Hong Kong (Berthouly et al., 2008) This breed showed the highest body weight at 16 weeks of age (Chang et al., 2012) Selection for a specific trait has resulted in a reduction of genetic variation (Toro
et al., 2011).Chang et al (2012)showed that Hsin-Yi, Shek-Ki and Hua-Tung males exhibited a better heat tolerance due to a lower panting rate than observed in others In addition, Hsin-Yi re-sponded to the highest antibody levels from Infectious Bursal Disease (IBD) vaccine The Quemoy exhibited high antibody re-sponse to low pathogenic avian influenza H6N1 virus, Newcastle Disease and IBD vaccines
4 Conclusions The Shek-Ki breed is of high priority for conservation con-sidering risk and utility, the Hua-Tung breed is of high priority considering risk and diversity, and the Quemoy breed is of high priority considering diversity and utility Then, the Nagoya breed may be of high priority considering between-breeds diversity, and the Hsin-Yi, B and L2 lines could be considered for conservation on the basis of utility only Thus, this study of TCP populations shows how different types of data can be combined to define conserva-tion priorities considering risk, diversity, or utility of local breeds
Conflict of interest statement
No actual or potential conflict of interest in relation to this ar-ticle exists
Acknowledgments
We sincerely appreciate the chicken caretaker at NCHU ex-perimental farm and graduate students for their assistance in pedigree recording We also would like to thank two anonymous
Table 5
Loss or gain of genetic diversity, contributions to allelic richness and aggregate diversity for each of the eight Taiwan conserved chicken breeds.
GD W , change in within-population genetic diversity after removing population i; GD B , change in between-population genetic diversity after removing population i; GD G , change in global diversity after removing population i; C S , a contribution to within-population genetic diversity; C D , a between-population genetic diversity; C T , Total diversity; CW, contribution to within-population diversity; CB, contribution to between-population diversity; and D, aggregate diversity (in percentage).
M.-H Pham et al / Livestock Science 184 (2016) 85–91 90
Trang 7reviewers to revise the manuscript with several improvements.
References
Ballou, J.D., Lacy, R.C., 1995 Identifying genetically important individuals for
management of genetic variation in pedigreed populations In: Ballou, J.D.,
Gilpin, M., Foose, T.J (Eds.), Population Management for Survival and Recovery:
Analytical Methods and Strategies in Small Population Management Columbia
University Press, New York, NY, pp 76–111
Bennewitz, J., Eding, H., Ruane, J., Simianer, H., 2007 Selection of breeds for
con-servation In: Oldenbrook, K (Eds.), Utilization and Conservation of Farm
Ani-mal Genetic Resources, Wageningen Academic Publishers, Wageningen, The
Netherlands, pp 131–146.
Berthouly, C., Bed’Hom, B., Tixier-Boichard, M., Chen, C.F., Lee, Y.P., Laloë, D., Legros,
H., Verrier, E., Rognon, X., 2008 Using molecular markers and multivariate
methods to study the genetic diversity of local European and Asian chicken
breeds Anim Genet 39, 121–129
Boettcher, P.J., Tixier-Boichard, M., Toro, M.A., Simianer, H., Eding, H., Gandini, G.,
Joost, S., Garcia, D., Colli, L., Ajmone-Marsan, P., Consortium, G., 2010
Objec-tives, criteria and methods for using molecular genetic data in priority setting
for conservation of animal genetic resources Anim Genet 41 (Suppl 1),
S64–S77
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
Caballero, A., Toro, M.A., 2000 Interrelations between effective population size and
other tools for management of conserved populations Genet Res 75, 331–343
Caballero, A., Toro, M.A., 2002 Analysis of genetic diversity for the management of
conserved subdivided populations Conserv Genet 3, 289–299
Cervantes, I., Goyache, F., Molina, A., Valera, M., Gutiérrez, J.P., 2011 Estimation of
effective population size from the rate of coancestry in pedigreed populations.
J Anim Breed Genet 128, 56–63
Cervantes, I., Goyache, F., Molina, A., Valera, M., Gutiérrez, J.P., 2008 Application of
individual increase in inbreeding to estimate effective sizes from real pedigrees.
J Anim Breed Genet 125, 301–310
Chang, C.S., Chen, C.F., Berthouly-Salazar, C., Chazara, O., Lee, Y.P., Chang, C.M.,
Chang, K.H., Bed’Hom, B., Tixier-Boichard, M., 2012 A global analysis of
mole-cular markers and phenotypic traits in local chicken breeds in Taiwan Anim.
Genet 43, 172–182
Chao, C.H., Lee, Y.P., 2001 Relationship between reproductive performance and
immunity in Taiwan country chickens Poult Sci 80, 535–540
Chapuis, M.P., Estoup, A., 2007 Microsatellite null alleles and estimation of
popu-lation differentiation Mol Biol Evol 24, 621–631
Chen, C.F., Shiue, Y.L., Yen, C.J., Tang, P.C., Chang, H.C., Lee, Y.P., 2007 Laying traits
and underlying transcripts, expressed in the hypothalamus and pituitary gland
that were associated with egg production variability in chickens
Ther-iogenology 68, 1305–1315
Derban, S., Foulley, J.-L., Ollivier, L., 2002 WEITZPRO: Software for Analysing
Ge-netic Diversity INRA, Paris
EAAP, 1998 Assessment of the degree of endangerment of livestock breeds.
Working group on Animal Genetic Resources, In: Proceedings of the 49th
An-nual Meeting of European Association for Animal Production, Warsaw, Poland.
EAAP Publication, Wageningen Academic Publishers, Wageningen, The
Netherlands.
Engelsma, K.A., Calus., M.P.L., Bijma, P., Windig, J.J., 2010 Estimating genetic
di-versity across the neutral genome with the use of dense marker maps Genet.
Sel Evol 42, 12
Engelsma, K.A., Veerkamp, R.F., Calus, M.P.L., Bijma, P., Windig, J.J., 2012
Pedigree-and marker-based methods in the estimation of genetic diversity in small
groups of Holstein cattle J Anim Breed Genet 129, 195–205
Falconer, D.S., Mackay, T.F.C., 1996 Introduction to Quantitative Genetics Longman
Group, Essex, UK
Fanatico, A.C., Owens, C.M., Emmert, J.L., 2009 Organic poultry production in the
United States: Broilers J Appl Poult Res 18, 355–366
FAO, 2000 World Watch List for Domestic Animal Diversity, Scherf, B.D (Eds.).
Third Edition, Rome.
FAO, 2011 Molecular Genetic Characterization of Animal Genetic Resources FAO
Animal Production and Health Guidelines, Rome (No 9)
FAO, 2014 Status and trends of animal genetic resources Commission on genetic
resources for food and agriculture Eighth Session Rome, 26–28 November
2014.
Goyache, F., Álvarez, I., Fernández, I., Pérez-Pardal, L., Royo, L.J., Lorenzo, L., 2011.
Usefulness of molecular-based methods for estimating effective population size
in livestock assessed using data from the endangered black-coated Asturcĩn
pony J Anim Sci 89, 1251–1259
Grundy, B., Villanueva, B., Woolliams, J.A., 1998 Dynamic selection procedures for
constrained inbreeding and their consequences for pedigree development.
Genet Res 72, 159–168
Gutiérrez, J.P., Cervantes, I., Goyache, F., 2009 Improving the estimation of realized
effective population sizes in farm animals J Anim Breed Genet 126, 327–332
Gutiérrez, J.P., Cervantes, I., Molina, A., Valera, M., Goyache, F., 2008 Individual
increase in inbreeding allows estimating realised effective sizes from pedigrees Genet Sel Evol 40, 359–378
Gutiérrez, J.P., Goyache, F., 2005 A note on ENDOG: a computer program for ana-lysing pedigree information J Anim Breed Genet 122, 172–176
Gutiérrez, J.P., Royo, L.J., Álvarez, I., Goyache, F., 2005 MOLKIN v2.0: a computer program for genetic analysis of populations using molecular coancestry in-formation J Hered 96, 718–721
Hill, W.G., 1981 Estimation of effective population size from data on linkage dis-equilibrium Genet Res 38, 209–216
Lacy, R.C., 1989 Analysis of founder representation in pedigrees: founder equiva-lent and founder genome equivaequiva-lents Zoo Biol 8, 111–123
Lacy, R.C., 1995 Clarification of genetic terms and their use in the management of captive populations Zoo Biol 14, 565–578
Langella, O., 1999 POPULATIONS 1.2.32 Copyright© by CNRS UPR9034, France Lee, Y.P., 2006 Taiwan country chicken: a slow growth breed for eating quality In: Liao, C.W., Shih, B.L., Lee, M.L., Hsu A.L and Cheng Y.S (Eds.), Symposium 7–
10 November 2006, Scientific Cooperation in Agriculture between Council of Agriculture, Taiwan, R.O.C and Institut National de Recherche Agronomique, France, Technical Bulletin of Livestock Research Institute 103, pp 121–132.
Lenstra, J.A., Groeneveld, L.F., Eding, H., Kantanen, J., Williams, J.L., Taberlet, P., Ni-colazzi, E.L., Sưlkner, J., Simianer, H., Ciani, E., Garcia, J.F., Bruford, M.W., Aj-mone-Marsan, P., Weigend, S., 2012 Molecular tools and analytical approaches for the characterization of farm animal genetic diversity Anim Genet 43, 483–502
Leroy, G., Mary-Huard, T., Verrier, E., Danvy, S., Charvolin, E., Danchin-Burge, C.,
2013 Methods to estimate effective population size using pedigree data: ex-amples in dog, sheep, cattle and horse Genet Sel Evol 45, 1
Meuwissen, T.H.E., 2009 Towards consensus on how to measure neutral genetic diversity? J Anim Breed Genet 126, 333–334
Nei, M., 1987 Molecular Evolutionary Genetics Columbia Univ Press, New York,
NY, pp 1–512
Nei, M., Tajima, F., Tateno, Y., 1983 Accuracy of estimated phylogenetic trees from molecular data J Mol Evol 19, 153–170
Ollivier, L., Foulley, J.L., 2005 Aggregate diversity: new approach combining within-and between-breed genetic diversity Livest Prod Sci 95, 247–254
Petit, R.J., Mousadik, A.E., Pons, O., 1998 Identifying populations for conservation
on the basis of genetic markers Conserv Biol 12, 844–855
Pham, M.H., Berthouly-Salazar, C., Tran, X.H., Chang, W.H., Crooijmans, R.P.M.A., Lin, D.Y., Hoang, V.T., Y.P., L., Tixier-Boichard, M., Chen, C.F., 2013a Genetic diversity
of Vietnamese domestic chicken populations as decision-making support for conservation strategies Anim Genet 44, 509–521
Pham, M.H., Chang, W.H., Berthouly-Salazar, C., Lin, D.Y., Yungrahang, S., Wang, C.C., Lee, Y.P., Tixier-Boichard, M., Chen, C.F., 2013b Genetic characterization of Taiwan commercial native chickens ascertained by microsatellite markers J Poult Sci., 290–299
Pham, M.H., Tran, X.H., Lee, Y.P., Lin, D.Y., Pham, D.L., Hoang, V.T., Tixier-Boichard, M., Chen, C.F., 2012 Genetic diversity of the major histocompatibility complex region in Vietnamese local chickens using the LEI0258 microsatellite marker J Anim Sci Technol 34, 11–19
Siliĩ, L., Fernández, A., Mercadé, A., Martin-Palomino, P., Lĩpez, M.A., Rodrigáđez, J., Ovilo, C., 2010 Measuring inbreeding in a closed pig strain from high-density SNPs genotypes In: Proceedings of the 9th World Congress Genetics Applied Livestock Production Congress, Leipzig, Germany, 1–6 August 2010.
Tixier-Boichard, M., Bordas, A., Rognon, X., 2009 Characterisation and monitoring
of poultry genetic resources Worlds Poult Sci J 65, 272–285
Toro, M.A., Barragán, C., Ĩvilo, C., Rodrigađez, J., Rodriguez, C., Siliĩ, L., 2002 Esti-mation of coancestry in Iberian pigs using molecular markers Conserv Genet.
3, 309–320 Toro, M.A., Fernández, J., Caballero, A., 2006 Scientific basis for policies in con-servation of farm animal genetic resources The 8th World Congress on Ge-netics Applied to Livestock Production, Belo Horizonte, MG, Brasil, August 13–
18, 2006.
Toro, M.A., Meuwissen, T.H.E., Fernández, A., Shaat, I., Mäki-Tanila, A., 2011 As-sessing the genetic diversity in small farm animal populations Animal 5, 1669–1683
VanRaden, P.M., Tooker, M.E., 2007 Methods to explain genomic estimates of breeding value J Dairy Sci 90 (Suppl 1), S374
Waples, R.S., 2006 A bias correction for estimates of effective population size based
on linkage disequilibrium at unlinked gene loci Conserv Genet 7, 167–184
Waples, R.S., Do, C., 2008 LDNe: A program for estimating effective population size from data on linkage disequilibrium Mol Ecol Notes 8, 753–756
Waples, R.S., Do, C., 2010 Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution Evol Appl 3, 244–262
Weitzman, M.L., 1993 What to preserve? An application of diversity theory to crane conservation Q J Econ 108, 157–183
Wright, S., 1931 Evolution in Mendelian populations Genetics 16, 97–159
Wright, S., 1969 Evolution and the Genetics of Populations, Vol 2: Theory of Gene Frequencies University of Chicago Press, Chicago, IL
Zanetti, E., De Marchi, M., Dalvit, C., Cassandro, M., 2010 Genetic characterization of local Italian breeds of chickens undergoing in situ conservation Poult Sci 89, 420–427