Caballero A., Toro M.A. The Border Collie dogs are bred based on a closed herd book which predisposes to an increased inbreeding level of the population. government site. Intervals within the show and working lines were similar; however, the mean age of the father when the offspring was born was somewhat lower in the mixed line (sireson path: 2.71 years, siredaughter path: 4.33 years). 8600 Rockville Pike Calboli F.C.F., Sampson J., Fretwell N., Balding D.J. In addition, fixation indices (FIS, FST) were calculated to detect the reduction of heterozygosity among subpopulations and individuals for measuring the total population differentiation [7]. Gutirrez J.P., Cervantes I., Molina A., Valera M., Goyache F. Individual increase in inbreeding allows estimating realised effective sizes from pedigrees. Demographic parameters of the border collie breed in Hungary. Boichard D., Maignel L., Verrier E. The value of using probabilities of gene origin to measure genetic variability in a population. The Border Collie is considered as one of the most intelligent dog breeds, and originated from the England Northumbria region. When estimating the proportion of each dogs genome that was identical by descent in an ancestor to alleles identical by descent for the first time in that dogs linage by the gene dropping method, the F_KAL and F_KAL_NEW showed similar results. Caballero A., Toro M.A. These characteristics were defining the basics of todays collecting style herding. about navigating our updated article layout. Regarding the Hungarian Border Collie population, the first two females were imported in the country in 1995. Ancestral inbreeding coefficients were added to determine if inbred alleles in the past may have influenced the characterisations of these different phenotypes (Table 4). In addition, genetic variability within the breed is decreasing due to a lack of suitable mating plans and the education of the breeders who are repeatedly choosing to breed animals with similar show-related characteristics. Gutirrez J.P., Goyache F. A note on ENDOG: A computer program for analysing pedigree information. Due to the unequal contribution of the breeding animals to the next generation, the effective population size is always smaller compared to the exact population size. The constructed pedigree file consisted of 13,339 individuals, of which 1566 dogs (born between 2010 and 2016) composed the alive reference population which was active from breeding perspective. For the calculation of the fixation indices, coancestry and kinship distance were used [8,9], using the following equations: where f is the mean coancestry for the metapopulation; F is the mean inbreeding coefficient for the metapopulation; and D is the average genetic distance between the subpopulations. For the generation intervals, the results are not surprising as the reproductive life of sires is usually longer compared to dams. The breeds name is related to the words border (between England and Scotland), coal (basic color), and koolie (useful) [1,2]. In Hungary, the working line is at the greatest risk in terms of the number of breeding animals and the number of litters. Interrelations between effective population size and other pedigree tools for the management of conserved populations. Kalinowski S.T. Animals : an Open Access Journal from MDPI, http://creativecommons.org/licenses/by/4.0/. However, the contrasts in dog selection may increase the genetic distance. Unfortunately, this decreasing trend may coincide with the loss of genetic variability and with the appearance of genetic diseases [14]. F: inbreeding coefficient; Gen_eq: number of complete generation equivalents. Data curation, V.. The inbreeding coefficients were also adjusted in the three lines. Van der Beek S., Nielen A.L., Schukken Y.H., Brascamp E.W. Analysis of genetic diversity for the management of conserved subdivided populations. Descriptive statistics of the generation interval (T) for the reference population (20102016). sharing sensitive information, make sure youre on a federal Due to the changing breed standards and the requirements of the potential buyers, the effective population size substantially decreased between 2010 and 2016. The presence of preferential breeding can be shown by calculating the ratio of fe and fa. Inbreeding (F) and average relatedness (AR) of the reference population. Thus, the reference population was dissected according to the existing lines. and transmitted securely. Baumung R., Farkas J., Boichard D., Mszros G., Slkner J., Curik I. The size of the active breeding population has decreased dramatically in the past years. Leroy G., Mary Huard T., Verrier E., Danvy S., Charvolin E., Danchin-Burge C. Methods to estimate effective population size using pedigree data: Examples in dog, sheep, cattle and horse. There are three specific lines within the breed worldwide, which are also represented in Hungary, such as the show line, the working line, and the so-called mixed line originating from Australia and New-Zealand. The generation interval was calculated as the average age of parents at the birth of their progeny kept for the reproduction, and it was computed for all four parentprogeny pathways (Table 2) represented in the total reference population and per line. Ancestral inbreeding coefficients in subpopulations (%). However, the dog-keeping culture is improving; there are still many backyard breeders who are selling puppies at often half of the cost of the breeders price, resulting in a huge border collie mix population. Similar results were found in the Nova Scotia Duck Tolling Retriever and the Lancashire Heeler dog breeds [21], and for several French dog breeds [18,19]. Genetic diversity and population structure of the synthetic Pannon White rabbit revealed by pedigree analyses. The breed was registered by the British Kennel Club. Moreover, this non-random mating is able to increase inbreeding depression (bringing alleles to a homozygous state), affecting the future genetic health of the breed. Bokor . Equihun Pedigree BuilderMS Access application specifically developed for genealogy records process. Cecchi F., Paci G., Spaterna A., Ragatzu M., Ciampolini R. Demographic approach on the study of genetic parameters in the dog Braque Francais type Pyrnes Italian population. Licensee MDPI, Basel, Switzerland. 2004. Genetic differences among the existing lines calculated by fixation indices are not significant; nonetheless ancestral inbreeding coefficients are able to show contrasts. str., Hungary; uh.ek@navtsi.ygan, 2Department of Hippology, Kaposvr, Kaposvr University, Kaposvr, H-7400, 40, Guba S. The main finding of the study was that there is a detectable genetic divergence between the show and working line. The new PMC design is here! Then, the database was dissected into three groups. Effective population size (Ne) of the reference population. For the first 15 generations, the pedigree completeness was 99.6%, decreasing to 87.6% by the 40th generation. The maximum and average number of complete generation equivalents were 25.04 and 4.47, respectively. Obtaining the status show champion was however only possible after passing the so-called working exam in several countries. This pedigree quality is only comparable to that of thoroughbred horses and Pannon White rabbit populations [24,25]. ; Formal analysis, V.. The structure of the Hungarian Border Collie population was characterized by the following parameters: All these parameters were explained in detail by [5]; therefore equations related to the listed parameters will not be repeated here. The One of the reasons for decreasing the effective population size is that most of the puppies born in Hungary are sold abroad due to the lack of suitable owners for the breed. Contrary to his conspecifics, his herding work was performed without barking, carefully approaching the sheep and controlling the flock with an intensive stare, or eye. The aim of the study was to map the current population in Hungary and determine the possible inbreeding levels in and between the different subpopulations. The .gov means its official. Collection of titles requires many years, so the preferred breeding males are usually older than the females. The pedigree dataset of the Hungarian Border Collie population was constructed using available electronic herd books and pedigrees from Hungarian breeders. Kalinowski S.T., Hedrick P.W., Miller P.S. These websites could be searched but their content could not be downloaded, and therefore all genealogy data had to be retyped manually. Importation of breeding dogs could be a solution to this problem; on the other hand, breeding standards are slightly different between countries, and thus a collaboration is required between breeding organizations and scientists to improve the health of the next generation. Received 2019 Mar 21; Accepted 2019 May 13. Federal government websites often end in .gov or .mil. Breeding of the Collie-type dogs began in the British Islands in the 19th century in order to help the shepherds in gathering, driving, singling, penning, loading in trailers, and shedding races. official website and that any information you provide is encrypted The appearance of dog breeds is constantly changing, for many reasons. N: number of individuals in the reference population; T: generation interval; SD: standard deviations; SE: standard errors of means. The site is secure. Unpublished. PMC legacy view The present population is not consistent; the number of registered breeders is 154. Moreover, ancestral inbreeding coefficients proposed by the authors of [10,11,12] and determined with GRain 2.0 software [13] were used to obtain whether these distinct measurements for inbreeding are able to describe the differences between the lines. Inbreeding Depression in the Spekes Gazelle Captive Breeding Program. La Manna V., Lasagna E., Ceccobelli S., Di Lorenzo P., De Cosmo A.M., Attard G., Sarti F.M., Panella F., Renirei C. Genetic Differentiation Between Segugio DellAppeinnino and Segugio Maremmano Dog Breeds Assessed by Microsatellite Markers. The name Border Collie was first used by the International Sheep Dog Society (ISDS) in 1915 in order to distinguish this breed from the Smooth and Bearded Collies, which at the beginning had similar breeding aspects. Analogous fixation indices were measured studying native Italian hunting dog breeds with microsatellite markers [3]. Besides, accommodating to the breed standards also decreases the effective population size. A slow but continuous increase of the inbreeding coefficient based on the increasing complete generation equivalent was obvious (Figure 2). ; Writingoriginal draft, V.. Trends in the probability of gene origin fe, fa50, and their ratios are presented in Table 1. The following information was entered: After exporting the pedigree records their correctness was checked, pedigree analysis was performed applying ENDOG software [5]. Pedigree data of the Border Collie dog breed were collected in Hungary to examine genetic diversity within the breed and its different lines. National Library of Medicine N: Number of individuals; F: inbreeding coefficient; F_BAL: Ballous formula to ancestral inbreeding; F_KAL: Kalinowskis formula to ancestral inbreeding; F_KAL_NEW: Kalinowskis new formula to ancestral inbreeding; AR: average relatedness. The lower length of the mixed-line generation interval can be attributed to the fact that these dogs are bred with lower show and working performance. Since the final objectives for dogs in shows and sports require different anatomical structures, the importance of these lines is outstanding. ; Software, .B. The observed small ratio of fa and fe of the Hungarian Border Collie population can be explained by its closed herd book, intense selection for appearance, and by the favoritism of some relevant individuals. For the determination of the cumulative proportion of the genome that was exposed to inbreeding effects, ancestral inbreeding (F_BAL) was calculated in the subpopulations. This research was funded by Orszgos Tudomnyos Kutatsi Alapprogramok, grant number 128177. In many populations, all estimates related to the probability of gene origin decreased the most during the first years. This mixed line combines the appearance of show dogs (heavier bones, elegant head, thicker coat) with the energy and stamina of the working-lined dogs, with the objective of use in search and rescue, therapy, or sports. Figure 3. represents the effects to the subdivision on the reference population, highlighting that the studied lines started to separate; nonetheless this is not statistically proven. The use of specific lines within one breed was previously reported in France [3], where more than 49% of the breeders claimed to use line breeding in practice. In dog breeding, mating of close relatives is a common practice, where the objective is to create an outstanding individual [22]; however, after few generations, the raised inbreeding level escalates juvenile mortality [23]. Evaluation of genetic, common-litter, and within-litter effects on preweaning mortality in a birth cohort of puppies. National Excellence Program of the Ministry of Human Capacities, grant number NKP-18-3. ; Writingreview & editing, I.N. Compared to a great number of founders, a large part of the genetic variability is maintained based on only eight ancestors (Table 1). In the calculation of the subdivision of the lines (Table 5), the within-variety fixation index (FIS) was 0.36%, showing that mating within lines was not random; this is in contrast to sheep and horse breeds, where this value is negative [17], showing that individuals in farm animal species are less related. Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. The Shepherds of Brittain: Scenes from a Shepherds Life. Generation intervals varied between 4.09 and 4.71 years, where the sire paths were longer due to the later initial age of breeding in males compared to females. Thus, the main objectives for breed selection, in descending order, were herding instinct, acceptance of human guiding, and speed. Fij: mean coancestry within subpopulations; si: self-coancestry; Dij: Neis minimum distance; FST: inbreeding caused by the differentiation of the subpopulation; FIS: inbreeding coefficients within the subpopulations. Small values signal the so-called bottleneck effect [20]. It is also a common practice for dog breeders to choose sires and dams with a common ancestor to fix some specific traits in the appearance or working ability. In the long run, continuous selection for different purposes such as for show and work may disrupt the breed. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (, Number of founders (f: ancestors with two unknown parents), Effective number of founders (fe: the number of equally contributing founders that would be expected to produce the same genetic diversity as in the population under study), Effective number of ancestors (fa: similar to fe but replacing the contributions of founders with the marginal contributions of ancestors), Number of ancestors responsible for 50% of the genetic variability (fa50), Generation interval (average age of parents at the birth of their progeny kept for reproduction), Pedigree completeness (proportion of its known ancestors per generation), Inbreeding coefficient (the probability that the two alleles at any locus in an individual are identical by descent), Average relatedness (the probability that an allele randomly chosen from the whole population belongs to a given animal), Effective populations size (realized effective population size) from an individual increase of inbreeding [, Border Collie, inbreeding, pedigree analysis, population size, subpopulations. The number of founders was 894, but eight individuals were responsible for contributing 50% of the genetic variability. Leroy G., Rognon X., Varlet A., Joffrin C., Verrier E. Genetic variability in French dog breeds assessed by pedigree data. Maintaining genetic diversity in order to create productive and healthy offspring without increasing the genetic load is the key to maintaining small populations. Association between inbreeding coefficient and complete generation equivalents in the total population. The Border Collie breed has several lines depending on sport, show, or work requirements, with closed breeding practices within these lines in recent decades. However, there are many dogs in the country without a pedigree. Adding ancestral inbreeding coefficients, Ballous formula showed that individuals in the working line had less probability of inheriting an allele which had undergone inbreeding in the past at least once than individuals in the show and the mixed lines. Looking at the observed ratio of fa and fe it can be concluded that the Hungarian Border Collie population has suffered very strong gene loss. str., Hungary; uh.ek@dapra.rokob. The first public sheep herding event took place at Wales in 1873, where Old Hemp, one of the founders of the breed, appeared. Genetic similarities within the population. Furthermore, both Kalinowskis formulas show that the working line suffered less inbreeding in the past few generations. The reference population had a pedigree completeness of 99.6% up to 15 generations and an inbreeding coefficient of 9.86%. The reference population was composed of 1566 dogs (703 males and 863 females). The https:// ensures that you are connecting to the The database was based on available herd books dating from the development of the breed (in the late 1800s) to the present day. Bokor ., Jns D., Ducro B., Nagy I., Bokor J., Szabari M. Pedigree analysis of the Hungarian Thoroughbred population. Nagy I., Curik I., Radnai I., Cervantes I., Gyovai P., Baumung R., Farkas J., Szendr Z. The inbreeding coefficients of the different lines depending on the total generation equivalent, where F is the inbreeding coefficient of an individual and GenEqu is the number of complete generation equivalents. Therefore, determining annual numbers was not possible. Herding Dogs: Their Origins and Development in Britain. Hence, the objective of this study was to analyze the effects of closed breeding on the population structure of the Border Collie dog breed in Hungary and examine the genetic diversity within and between the subpopulations. Comparing this result to other populations, the medium value (0.75) of the fa/fe ratio of the Braque Francais dog population shows a more balanced use of animals for breeding and an absence of a bottleneck in that population [18]. Show line, Mixed line, Working line, Total population. Evolution and the Genetics of Populations: Variability within and among Natural Populations. Before HHS Vulnerability Disclosure, Help Evolution of the inbreeding coefficient and the average relatedness of the reference population is provided in Table 3. The created Hungarian Border Collie pedigree dataset contained 13,339 individuals (5649 males and 7750 females). First, the reference population was defined as the living and active animals (from the perspective of breeding) born between 2010 and 2016. Similar tendencies were reported in several dog breeds [15]. Bethesda, MD 20894, Web Policies The decreasing tendency of the effective population size points out a trend that dog owners prefer not to buy from registered breeders. The decrease of the average inbreeding coefficients between 2011 and 2014 can be explained by the intense import of breeding animals. As the population size of the Border Collie breed in Hungary is relatively large, the increase of the inbreeding level was relatively small (10% per 23 years). f: number of founders; fg: equivalent number of founders; fe: effective number of founders; fa: effective number of ancestors; fa50: number of ancestors responsible for 50% of the genetic variability. An official website of the United States government. Evolutionary and Statistical Properties of Three Genetic Distances. If fe is larger compared to fa, the population suffers from gene loss and consequently a decrease in genetic variation [16]. In the present study, the sire paths were longer as the males were kept in breeding for longer ages than females and there is also a tendency for breeders to prefer to use males with more show and sport results rather than males with few titles even if they could increase the genetic variability within the breed. It can be seen that despite the proportion of registered breeders, dog owners prefer not to buy purebred dogs, and thus most of the pups born in Hungary are exported to other countries. GRAIN: A computer program to calculate ancestral and partial inbreeding coefficients using a gene dropping approach. ; Methodology, I.N. N: Number of individuals; F: inbreeding coefficient; F_BAL: Ballous formula for ancestral inbreeding; F_KAL: Kalinowskis formula for ancestral inbreeding; F_KAL_NEW: Kalinowskis new formula to ancestral inbreeding; AR: average relatedness. Leroy G., Baumung R. Mating practices and the dissemination of genetic disorders in domestic animals, based on the example of dog breeding. Accessibility Then, the available genealogy information of these dogs was traced back and was recorded, creating the pedigree of the whole population from the late 1800s to the present day. ; Project administration, I.N. Ballou J.D. The authors declare no conflict of interest. The differences between the show and working lines regarding Ballous formula are 20.4%; in addition the working line also differs from the mixed line by 20%. Calculations for ancestral inbreeding were previously used by the authors of [10,11,12]. The length of the generation interval (T) can be substantially divergent across different breeds. 1Department of Animal Sciences, Kaposvr University, Kaposvr, H-7400, 40, Guba S. This so-called line breeding tries to avoid closely-related mating; however, the breeding association sometimes permits it. Learn more From the 1860s exhibitions became more and more popular, and their appearance was more consistent. The genealogy records used in this study were created using the software Equihun Pedigree Builder [4]. In the total population, only 2.77% of the matings were highly inbred (0.16% between full-sibs, 1.74% between half-sibs, and 0.87% between parentoffspring). Because inbreeding coefficients are always dependent on the length and on the completeness of the pedigree the inbreeding coefficients were plotted on the complete generation equivalents [16]. The breed is subdivided by phenotype, showing a thicker coat, harmonic movement, a wide skull, and heavier bones for the show type, and a thinner or sometimes short coat and smaller body for the working line, while the mixed line is quite heterogeneous (a combination of the above). Inbreeding coefficients differed among the studied lines; the average inbreeding coefficient was 4.9% in the reference population of the working line, while it reached 10.51% and 11.03% between 2010 and 2016 in the mixed and show lines, respectively. Trends in the realized effective population size are presented in Figure 1. Unfortunately, in this study, the analyzed period covered more than a century. However, this line represents the look and the original function of the breed. In the reference population (fa/fe ratio: 0.17), the overall FST was 2.6%, with decreasing heterozygosity at the subpopulation level; however the genetic differences are still not significant, despite the diversity of the pheotype of the lines in the past 20 years. FOIA In addition, inbreeding coefficient was also calculated by the method of [11] by dividing inbreeding into two parts, based on whether part of the identical alleles were inbred in the past (F_KAL) or became inbred in recent generations (F_KAL_NEW). Careers. Mki K. Population structure and genetic diversity of worldwide Nova Scotia Duck Tolling Retriever and Lancashire Heeler dog populations. The Border Collie breed was officially recognized by the Fderation Cynologique Internationale (FCI) in 1977, and the valid official breed standard was published in 1987 when selection for appearance began. In case of working and show dogs, there are slight differences among breed standards between countries; thus, import of breeding animals is not always appropriate from the breeders point of view. Maignel L., Boichard D., Verrier E. Genetic variability of French dairy breeds estimated from pedigree information. Similar findings were also reported in the French Beauceron and Braque Francais dog populations [18,19]. will also be available for a limited time. Population Structure and Inbreeding from Pedigree Analysis of Purebred Dogs. For pedigree completeness, the obtained values show that the available electronic herd books register all ancestors, and that the Hungarian Border Collie population has an exceptionally long and complete pedigree. To maintain variability, the genetic contribution of some preferred males could be limited by mating schemes in order to help the breeders. Only comparable to that of thoroughbred horses and Pannon White rabbit revealed by pedigree analyses 1995. 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