PEDIGREE ANALYSIS OF A RED FOX (VULPES VULPES) POPULATION
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Ann. Anim. Sci., Vol. 21, No. 2 (2021) 457–468 DOI: 10.2478/aoas-2020-0078
Pedigree analysis of a red fox (Vulpes vulpes)
population* *
Patrycja Grzybek1, Piotr Przysiecki2, Andrzej Filistowicz3, Jan Dobrzański1, Tomasz Szwaczkowski1♦
1
Department of Genetics and Animal Breeding, Poznan University of Life Sciences,
Wojska Polskiego 28, 60-637 Poznań, Poland
2
Higher School of Agriculture and Building in Leszno, 1 Maja 1, 64-100, Leszno, Poland
3
Institute of Animal Science, Wrocław University of Environmental and Life Sciences,
Norwida 25, 50-375 Wrocław, Poland
♦
Corresponding author: tomasz.szwaczkowski@up.poznan.pl
Abstract
Fur animal breeding has a long history. In many countries several fur animal species (including
the red fox) have been recognized as livestock. The aim of this study was to estimate the pedigree
parameters in the population of red fox on a Polish breeding farm. The data set consisted of infor-
mation on 39 434 individuals, including 18 697 females and 20 004 males (733 animals were of un-
known sex), from the years 1956–2016. The following pedigree parameters were estimated: aver-
age number of discrete generation equivalents, individual inbreeding coefficient, total and effective
number of founders, effective population size, average relationship, founder genome equivalent,
effective number of non-founders, and genetic diversity coefficient. The population size changed in
successive years. The average inbreeding level was 5.34% for the population as a whole, and 6.04%
for the inbred population. The estimated effective number of founders of the population was 84.18.
The founder genome equivalent, which indicates the anticipated loss of genetic diversity caused
by genetic drift, reached 9.59 in 2016 from an initial value of 34.22 in 1956. The loss of genetic di-
versity caused by the unequal contribution of the founder alleles did not change significantly over
the years. Generally, the results indicate the good pedigree structure (including pedigree complete-
ness) of the population studied. This implies reliable estimation of the inbreeding level, as one of
the most important parameters in the genetic improvement programme.
Key words: fur animals, genetic variability, inbreeding, pedigree completeness, effective popula-
tion size
The first red fox (Vulpes vulpes) farm was established in 1894 on Prince Edward
Island in Canada. Its owners, Charles Dalton and Robert Qulton, were pioneers in
the fur industry. After many years, they were able to obtain the first fox offspring
under breeding conditions, sell the skins of “less valuable” individuals, and leave
*Work financed from statutory activity of the Department of Genetics and Animal Breeding of the
Poznan University of Life Sciences.458 P. Grzybek et al.
the superior ones to continue breeding. The breeders achieved huge successes at fur
auctions, where prices for farm fox skins were four times higher than those obtained
by hunters (Colpitts, 1997).
The main reason for this high price disproportion was the success of long-term
selection aimed at improving the colour, size and quality of the coat. In addition,
other traits of the farm-bred fox, such as fertility, temperament and growth rate,
evolved significantly compared with its wild counterpart.
In a number of countries, fur animal species (including the red fox) have been
recognized as livestock and are an important part of the food and feed chain. Besides
creating income from the sale of skins, many fur species have the ability to consume
by-products of other industries, which otherwise would become a problematic form
of biowaste. Fur animal breeding in Poland has a long history. There are currently
more than seven hundred farms of fur animal species (officially recognized as live-
stock), including the red fox (Vulpes vulpes), Arctic fox (Alopex lagopus), American
mink (Neovison vison), European polecat (Mustela putorius), raccoon dog (Nyctere-
utes procyonoides), nutria (Myocastor coypus), chinchilla (Chinchilla lanigera) and
European rabbit (Oryctolagus cuniculus).
The genetic improvement programmes implemented at farms of red fox and other
fur animal species include both long-term selection and crossbreeding. Those pro-
grammes are typically aimed at increasing the size and quality of the coat (Wierzbicki
et al., 2007), and also include reproduction and behavioural traits in the breeding
strategy (Wierzbicki et al., 2004). It is well known that selection leads to a reduction
of genetic variability and an increase in the inbreeding level, while crossbreeding
stimulates genetic diversity, influencing the complexity of the pedigree structure.
Nowadays, pedigree information is widely used to assess genetic variability in
livestock (Melka and Schenkel, 2010; Borowska and Szwaczkowski, 2015), poul-
try (Graczyk et al., 2015) and wild animals (Skotarczak et al., 2018). Parameters
such as pedigree completeness (Curik et al., 2003), inbreeding coefficient (Wright,
1922) and genetic diversity (Ballou and Foose, 1996) are very important for breed-
ers. These parameters are an integral part of the genetic improvement of the popula-
tion, contributing to optimization of the selection of mating pairs. To our knowledge,
no prior reports on pedigree analysis of the Polish red fox population are available
in the literature.
The aim of this study was to estimate the pedigree parameters of the population
of red fox housed in a Polish breeding farm.
Material and methods
Data
The data set consisted of information about 39 434 individuals, including
18 697 females, 20 004 males and 733 animals of unknown sex, born between 1956
and 2016. The pedigree information studied concerned red foxes located at the Ba-
torówka breeding farm in Poland.Pedigree analysis of red foxes 459
The farm housed five colour varieties of foxes (silver, whiteneck, flaming, pearl
and pastel) and a white fox variety. The largest number of foxes was of silver colour
(86.07%), while 7.71% were whiteneck. The percentages of the other three varieties,
flaming, pearl and pastel, were 1.26%, 1.93% and 3.03%, respectively. In the years
1968–2012 the farm imported genetic material from Canada, Finland, Norway, and
the Soviet Union (until 1991). In total, 86 foxes were imported, most of which were
from Canada (Table 1).
Table 1. Foxes imported to the Batorówka farm in the years 1956–2016
Year Number Number Total Number of puppies born
of import of males of females number by imported parents
Canada 1985 18 22 40 623
Finland 1993 5 9 14 289
Norway 1997 6 6 12 459
Soviet Union 1968 10 10 20 239
For the first twenty years the data were collected in the form of paper documen-
tation. Subsequently, electronic registration was implemented. In 1996, a computer
software package called LISY (Chudoba et al., 1988) was implemented to estimate
the inbreeding coefficients. This enabled the optimization of matings in order to min-
imize the inbreeding level of the population.
Pedigree analysis
The following pedigree parameters were estimated for the population studied:
average number of discrete generation equivalents, individual inbreeding coefficient,
total and effective number of founders, founder genome equivalent, effective number
of non-founders, average relationship per year, effective population size per year,
and genetic diversity coefficient. These parameters are usually applied to character-
ize the genetic structure of a population based on pedigree information.
Pedigree completeness of the analysed population was calculated by means of
number of average discrete generation equivalents (ge), according to the following
formula given by Boichard et al. (1997):
nj
∑ ( 12 )
gij
ge =
j=1
where:
nj is the total number of ancestors of animal j in the reference population,
gij is the number of generations between animal j and its ancestor i.
The relationship between individuals and the average relationship per year were
calculated based on the additive relationship matrix (A).460 P. Grzybek et al.
The individual inbreeding coefficient (Fi), based on an algorithm developed by
Meuwissen and Luo (1992), was calculated using the additive relationship matrix
(A):
j
Fi = aii – 1, aii = ∑L D 2
ij jj
i=1
where:
aii is the ith diagonal element of the additive relationship matrix A,
Lij is the fraction of alleles derived from an ancestor,
Djj is the diagonal element of the matrix containing additive genetic variances
within the family.
Also, the average relationship per year was estimated based on the off-diagonal
elements of the matrix A.
The total number of founders (f) was determined as the number of ancestors with
both parents unknown.
The effective number of founders (fe) corresponds to the number of founders
which can produce a population with the same diversity of alleles as in the popula-
tion under study, assuming an equal contribution of all founders to each descend-
ant generation (Lacy, 1989). The parameter was calculated according to the formula
given by Lacy (1989):
[∑ p ]
f –1
2
fe = i
i=1
where:
pi is the proportion of alleles of the living, descendant population contributed by
founder i, calculated by the average relationship of the founder to each animal in the
population, and f is the total number of founders.
The founder genome equivalent (fge), which is related to the expected loss of
genetic diversity by genetic drift, was calculated using the formula (Caballero and
Toro, 2000):
1
fge = 2f
g
where:
fg is the average relationship between animals.
The effective number of non-founders is the parameter used to estimate the
amount of genetic diversity, reduced by random genetic drift accumulated in non-
founders’ generations (Caballero and Toro, 2000):
( )
–1
1 1
Nenf = –
fge fg
where:
fge, fg are as above.Pedigree analysis of red foxes 461
To measure genetic diversity in the reference population, a parameter called ge-
netic diversity (GD) is frequently used (Maignel et al., 1996). GD is calculated ac-
cording to the formula given by Lacy (1995):
1 1 1
GD = 1 – , DG’ = 1 – , GD’ – GD = 1 –
2fge 2fe 2Nenf
where:
GD is the loss of genetic diversity caused by unequal shares of founders’ alleles
in the population, and fge, fe, Nenf are as above.
Moreover, effective population size (Ne) was estimated using the formula given
by Wright (1931):
4NmNf
Ne =
Nm + Nf
where:
Nf is the number of females and Nm is the number of males.
These computations were performed using the CFC software package (Sargolzaei
et al., 2006).
Results
Changes of population size and pedigree completeness
Changes in the number of animals, the number of discrete generation equivalent
and the inbreeding level in the years 1956–2016 are presented in Figure 1.
Initially (in the years 1956–1966) an average number of 60 puppies were born
each year, while in later years this number increased as a consequence of a larger
number of breeding females. The population constantly increased during the next
two decades, on average by 276 individuals per year in 1967–1970, reaching its peak
(1 600) in 1984.
Reduction of the number of young animals introduced into the herd began after
2000. An increase took place after 2008, resulting from government payments to
dams of the white-necked variety covered by the genetic resources conservation pro-
gramme. The latest decrease in the number, around 2014, is due to the low interest in
fox skins on international markets.
The changes in effective population sizes over the years analysed are presented
in Figure 2. The values ranged from 32.97 in 1961 to 487.92 in 1981, and are subject
to similar fluctuations as the number of animals.462 P. Grzybek et al.
Figure 1. Number of all individuals on the farm, number of inbred animals, inbreeding level, average
number (per year) of discrete generation equivalent in the years 1956–2016
Figure 2. Effective population size (Ne) and average relationship level (R) in the years 1956–2016
This indicates that over the years the mating ratio and numbers of males and
females selected for reproduction have remained constant. The analysis of the popu-
lation showed that out of 39 434 individuals, 751 (357 sires and 394 dams) were
founders (with both parents unknown), and there was only one individual with one
known parent (with unknown sire). This means that 98.10% of individuals camePedigree analysis of red foxes 463
from two known parents. The average number of discrete generation equivalent in-
creased over time, reaching 17.4 in 2016 (Figure 1). The average value of this param-
eter for the whole population was 12.54, and the maximum value was 20.98.
Inbreeding level
The inbreeding coefficient ranged from 0% in 1956 to 34.7% in 1989 and showed
considerable fluctuations between individuals born in successive years. Until 1984,
both the number of total inbred animals (1600 individuals) and the average inbreed-
ing level in the population (6.33%) gradually increased (Figure 1). After that time,
these parameters declined. In 1991–1996 the inbreeding rate increased again, to reach
its maximum value (6.60%) in 1996. In 1964–1970 the largest increase in inbreeding
per generation was observed. The average inbreeding level for the studied popula-
tion was 5.34%, and in the inbred population it reached a slightly higher value of
6.04% (Table 2). The vast majority of individuals (88.48%) have non-zero inbreed-
ing coefficients (Table 3). A very high inbreeding rate of over 20% was observed in
92 individuals (0.23% of the population), which were born between 1975 and 1991.
The changes in average relationship per year (Figure 2) followed a similar pattern
to the average inbreeding level. The peak value was reached in 1997.
Table 2. Pedigree parameters of the red fox population
Parameter Value for the studied population
Number of individuals 39 434
Number of founders 751
Average complete generation equivalent 12.54
Maximum complete generation equivalent 20.98
Average inbreeding coefficient (%) 5.34
Average inbreeding coefficient of inbred animals (%) 6.04
Number of inbred animals 34 890
Table 3. Inbreeding level in the studied population
Inbreeding coefficient Fx (%) Number of individuals Percentage of individuals
0 4 544 11.52
0464 P. Grzybek et al.
Genetic contributions
The estimated effective number of founders (fe) of the population was 84.18. It
should be recalled that this value indicates the maximum number of different founder
genes transmitted to individuals in the population. The founder genome equivalent
(fge) indicates the anticipated loss of genetic diversity caused by genetic drift. Its
value was initially 34.22 and after 15 years stabilized at 7.50–9.59. The effective
number of non-founders (Nenf), which enables estimation of the size of genetic di-
versity reduced by the genetic drift accumulated in the generations of non-founders,
was 10.82.
The loss of genetic diversity caused by genetic drift was initially at a level of
98.53%. After 10 years from the establishment of the farm, this value gradually
decreased, finally reaching 93.34–94.24% (Figure 3). The loss of genetic diversity
caused by the unequal contribution of the founder alleles (GD') did not change sig-
nificantly over the years. Throughout the entire existence of the farm, it remained
within the range 98.88–99.57%.
Figure 3. Loss of genetic diversity due to genetic drift and unequal contribution of founders’ genes
(GD' – GD), genetic diversity caused by genetic drift (GD) and unequal contribution of founders’
genes (GD') in the analysed period
Discussion
The development of the studied population can be divided into several periods.
The increase in the number of individuals in the 1980s was caused by the develop-
ment of the farm (enlargement of its area, changes in nutrition, and imports of ani-
mals), which was closely related to the prevailing world fashion for fox pelts. In the
1990s the number of animals kept on the farm decreased. This was a time when the
interest of the fashion world in red fox pelts declined significantly. Also, the effectivePedigree analysis of red foxes 465
population size fluctuated over the years analysed, reaching its highest value of 487
in 1981. This value is similar to the highest value reported by Strandén and Peura
(2007) for the Finnish blue fox. Crucially for the preservation of genetic variability,
Ne never reached very low values, and after the first ten years it did not drop below
100, except in the last year analysed. This means that in terms of this parameter the
population was properly maintained, and the breeding schemes did not change much
over the years.
It is well known that the quality of pedigree information is dependent on the
number of identified ancestors across consecutive generations. Pedigree depth and
completeness have an influence on population parameters such as the inbreeding
coefficient. Also, the inbreeding level is considerably determined by the population
size and structure (Pjontek et al., 2012; Vostra-Vydrova et al., 2016).
One of the key requirements for genetic parameter analysis based on pedigrees
is their high degree of completeness (Curik et al., 2003). In the analysed population
the percentage of individuals with full pedigree data was 99.95%, while the aver-
age generation equivalent for the whole population was 12.54, indicating the good
quality of the pedigrees. In the first year of existence of the farm, the equivalent of
complete generations was small (2.4 ancestors) (Figure 1). The parameter increased
over time, reaching an average value of 13.3 in the 1990s and 17.4 in 2016. This
is a typical situation for first analysed generations, including base animals without
known parents. It should be noted that inbreeding may affect reproductive traits such
as litter size (in inbred populations, fewer juveniles are born) or survival. This situ-
ation was observed by Peura et al. (2004) in a population of Finnish Arctic foxes,
and by Wierzbicki et al. (2004) in a survey on the polar fox, which indicated that
with a 10% increase in the inbreeding level, the litter size decreases on average by
0.47 puppies. The reason for the smaller number of animals born may be a decrease
in reproductive capacity, associated with, for example, higher mortality of sperm.
Such a dependence was observed in a sheep population (Petrovic et al., 2013), where
sperm mortality was higher in a group of inbred rams than in the non-inbred animals.
A similar situation was reported in a study of American mink (Demontis et al., 2011).
This is important information for breeders, because such results indicate that an in-
crease in the level of inbreeding can cause a drop in income.
The inbreeding level in the population was relatively high compared with other
livestock species (5.34% for the entire population). By comparison, in Norwegian
and Finnish blue polar fox populations, the inbreeding level ranged between 1.3%
and 1.5% (Kempe and Strandén, 2018). It should be noted that in the studied popu-
lation the inbreeding level fluctuated considerably, and after reaching its maximum
value (6.60%) in 1996, it began gradually to decrease.
As shown in Figure 1, changes in the completeness of pedigrees and the inbreed-
ing level were recorded over time. It can be observed that pedigree completeness is
positively correlated with inbreeding level. Thus, as pedigree completeness increas-
es, estimates of inbreeding coefficients become more reliable. In case of unknown
parents, the inbreeding coefficients of progenies are assumed as zero. On the other
hand, the inbreeding level is reduced when unrelated animals are introduced from
other populations. The results obtained in the present study confirm the good genetic466 P. Grzybek et al.
monitoring of the analysed population. It should be recalled that the gene pool was
enriched by importing animals from abroad.
In determining genetic variability, it is important to take into account the partici-
pation of the founder alleles. It is also important for the population to be in a state of
genetic balance, which means that genetic variation should remain above 90% (Lacy,
1997). In the population studied, it was observed that the loss of genetic variation
due to unequal contribution of the founder alleles had no significant impact (it did
not exceed 1%). It is also important that the loss of genetic variability remained at
the same level over the past 20 years. The increasing difference between GD' and
GD may mean that the greater part of the reduced diversity resulted from the intense
use of too few males for breeding (Borowska and Szwaczkowski, 2015). A positive
trend in genetic variability (GD) can be observed at the end of the twentieth century.
This may have been affected by imported animals. Following the introduction of in-
dividuals from abroad (after 1998), this trend decreased. However, the participation
of foreign individuals in breeding was relatively small.
By contrast to the main species of farm animals such as cattle or chicken, fur ani-
mal breeding is subject to particular social pressure. This can considerably affect the
genetic structure of fur animal populations. The future of fox farms, as well as other
fur livestock, is significantly threatened. Despite the current fashion for a “healthy
lifestyle”, “ecology” and living in harmony with nature, society still chooses artifi-
cial forms of clothing over natural ones, whose distribution is also more beneficial
for the environment. Fur animal breeding has been banned in the majority of Europe-
an Union countries, and in the remaining countries there is ongoing public debate on
the subject. In spite of social education regarding this type of breeding, carried out by
a fur industry organization, there is still a general negative perception of fur farms. It
should be emphasized that the role of carnivore fur animal farms is extremely impor-
tant in relation to other types of animal-based production. Namely, fur animals feed
on by-products of animal origin, which means that this waste does not have to be
disposed of in such large amounts in ways that are far less environmentally friendly.
In addition, the need for waste to be disposed of by other industries would signifi-
cantly affect the economy: the costs of disposal would probably lead to the closure
of many farms of other animal species. In turn, opposition to fur animal breeding can
lead to a considerable decrease in the genetic diversity of both the Polish and world
red fox populations as a result of reduction of the scale of farming. This has been
the situation for years in nutria breeding, a species which supplied around 4 million
skins to international markets in the 1970s. Nowadays, in Poland there are only a few
thousand nutria of several colour varieties. However, all of them are included in the
genetic resource conservation programme.
Conclusions
The results of this study indicate the good pedigree structure (including pedi-
gree completeness) of the studied population. It confirms reliable estimation of the
inbreeding level, as the most important parameter in the genetic improvement pro-
gramme. Although the size of the population is quite large, loss of genetic diversity
caused by random genetic drift is also observed. Generally, it can be concluded thatPedigree analysis of red foxes 467
the studied population was subject to effective genetic management, especially in the
context of long-term selection.
Acknowledgments
We gratefully acknowledge the helpful comments of the anonymous reviewers
who contributed to the improvement of this manuscript.
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Received: 3 I 2020
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