Individual Inbreeding Coefficients Research Articles

Heterozygosity–fitness correlations in zebra finches: microsatellite markers can be better than their reputation

Numerous studies have reported associations between heterozygosity in microsatellite markers and fitness-related traits (heterozygosity-fitness correlations, HFCs). However, it has often been questioned whether HFCs reflect general inbreeding depression, because a small panel of microsatellite markers does not reflect very well an individual's inbreeding coefficient (F) as calculated from a pedigree. Here, we challenge this prevailing view. Because of chance events during Mendelian segregation, an individual's realized proportion of the genome that is identical by descent (IBD) may substantially deviate from the pedigree-based expectation (i.e. F). This Mendelian noise may result in a weak correlation between F and multi-locus heterozygosity, but this does not imply that multi-locus heterozygosity is a bad estimator of realized IBD. We examined correlations between 11 fitness-related traits measured in up to 1192 captive zebra finches and three measures of inbreeding: (i) heterozygosity across 11 microsatellite markers, (ii) heterozygosity across 1359 single-nucleotide polymorphism (SNP) markers and (iii) F, based on a 5th-generation pedigree. All 11 phenotypic traits showed positive relationships with measures of heterozygosity, especially traits that are most closely related to fitness. Remarkably, the small panel of microsatellite markers produced equally strong HFCs as the large panel of SNP markers. Both marker-based approaches produced stronger correlations with phenotypes than the pedigree-based F, and this did not seem to result from the shortness of our pedigree. We argue that a small panel of microsatellites with high allelic richness may better reflect an individual's realized IBD than previously appreciated, especially in species like the zebra finch, where much of the genome is inherited in large blocks that rarely experience cross-over during meiosis.

Efficient path-based computations on pedigree graphs with compact encodings

A pedigree is a diagram of family relationships, and it is often used to determine the mode of inheritance (dominant, recessive, etc.) of genetic diseases. Along with rapidly growing knowledge of genetics and accumulation of genealogy information, pedigree data is becoming increasingly important. In large pedigree graphs, path-based methods for efficiently computing genealogical measurements, such as inbreeding and kinship coefficients of individuals, depend on efficient identification and processing of paths. In this paper, we propose a new compact path encoding scheme on large pedigrees, accompanied by an efficient algorithm for identifying paths. We demonstrate the utilization of our proposed method by applying it to the inbreeding coefficient computation. We present time and space complexity analysis, and also manifest the efficiency of our method for evaluating inbreeding coefficients as compared to previous methods by experimental results using pedigree graphs with real and synthetic data. Both theoretical and experimental results demonstrate that our method is more scalable and efficient than previous methods in terms of time and space requirements.

Assessment of inbreeding depression for functional herd life in the South African Jersey breed based on level and rate of inbreeding

The objective of this study was to investigate the effect of inbreeding depression on functional herd life in the South African Jersey population based on individual level and rate of inbreeding. A pedigree file of the South African Jersey breed (n = 912 638) was obtained from the Integrated Registration and Genetic Information System (INTERGIS). The data included registered, grade and imported animals. The percentages of animals in the pedigree file with two, one and zero parents unknown were 22%, 18% and 60%, respectively. The inbreeding coefficient for each animal (Fi) and the rate of individual inbreeding (ΔFi) as an alternative measure of inbreeding that is adjusted for the depth of known pedigree were calculated. The effect of inbreeding on functional herd life in each of the first three lactations was estimated, using a singletrait sire model on data collected from 1985 to 2003. Three analyses for survival in each of the first three lactations were conducted. In the first analysis, in addition to fixed and random effects, an individual inbreeding coefficient (Fi) was fitted as a linear covariate. In the second analysis, the inbreeding coefficient was included as a discrete variable with the following classes of inbreeding: 0 < F ≤ 3.125, 3.125 < F ≤ 6.25, 6.25 < F ≤ 12.5 and F > 12.5. In the third analysis, the individual rate of inbreeding (ΔFi) was included in the model as a linear covariate. The level of inbreeding in the SA Jersey population showed a gradual increase for the period 1985 to 1994, while the period 1995 to 2003 showed a rapid increase. The current mean level of inbreeding (for the year 2010) is 4.85% with a minimum and maximum of 0 and 31.34%, respectively. The rate of inbreeding showed a gradual increase from 0.36% to 0.43% between 1985 and 2003. The average rate of inbreeding is currently (for the year 2010) at 0.55%. There was a significant unfavourable relationship between inbreeding and functional herd life in the first and second lactations. The effect of inbreeding was more pronounced in the second lactation for both measures of inbreeding. Based on the current level of inbreeding, the reduction in functional herd life in the first lactation can be estimated as 0.68%. The corresponding estimate for the second lactation is 1.70%. The results from the current study indicate that the current level or rate of inbreeding has reached levels that are detrimental to functional herd life. Therefore, individual inbreeding coefficients should be considered in addition to genetic merit when breeding decisions are made by Jersey breeders.Keywords: Inbreeding, longevity, survival, dairy cattle

Corrigendum to: Inbreeding and testicular abnormalities in a bottlenecked population of koalas (Phascolarctos cinereus)

Habitat destruction and fragmentation, interactions with introduced species or the relocation of animals to form new populations for conservation purposes may result in a multiplication of population bottlenecks. Examples are the translocations of koalas to French Island and its derivative Kangaroo Island population, with both populations established as insurance policies against koala extinction. In terms of population size, these conservation programs were success stories. However, the genetic story could be different. We conducted a genetic investigation of French and Kangaroo Island koalas by using 15 microsatellite markers, 11 of which are described here for the first time. The results confirm very low genetic diversity. French Island koalas have 3.8 alleles per locus and Kangaroo Island koalas 2.4. The present study found a 19% incidence of testicular abnormality in Kangaroo Island animals. Internal relatedness, an individual inbreeding coefficient, was not significantly different in koalas with testicular abnormalities from that in other males, suggesting the condition is not related to recent inbreeding. It could instead result from an unfortunate selection of founder individuals carrying alleles for testicular abnormalities, followed by a subsequent increase in these alleles' frequencies through genetic drift and small population-related inefficiency of selection. Given the low diversity and possible high prevalence of deleterious alleles, the genetic viability of the population remains uncertain, despite its exponential growth so far. This stands as a warning to other introductions for conservation reasons.

English

Although, Minshan A habitat is an area with one of the largest numbers of wild giant pandas ( Ailuropoda melanoleuca ); it may be threatened by habitat loss and fragmentation. In this study, 10 microsatellite DNA markers were used to assess population genetic structure of giant pandas from two critical reserves (Tangjiahe and Wanglang) in the Minshan A habitat. The results revealed high levels of genetic differentiation (F ST = 0.134) between the two populations. This differentiation was supported by the assignment tests using the Bayesian clustering method in STRUCTURE. The uniqueness of the populations was also supported by private alleles. This indicated a significant population fragmentation in Minshan A region. In addition, the high individual inbreeding coefficients for Wanglang indicated increased levels of homozygosity in the wild populations. Fortunately, those populations had high levels of genetic diversity. The average allelic richness (AR) and expected heterzygosity (H E ) were 4.520 and 0.689, respectively for Tangjiahe and 4.584 and 0.648 for Wanglang. Here, we propose an effective way to restore gene flow between the two isolated populations. Key words: Giant panda, microsatellite variation, genetic differentiation, habitat fragmentation, Minshan A habitat.

Population structure and effects of inbreeding on milk yield and quality of Murrah buffaloes

To provide data for conservation, selection, and expansion programs of buffalo herds, this study evaluated the history of a population of Murrah buffaloes based on population structure and the effect of inbreeding on accumulated 305-d milk yield (MY), fat yield (FY), protein yield (PY), mozzarella production (MProd), and somatic cell score (SCS). The usefulness of including the individual inbreeding coefficient (F) or individual increase in inbreeding coefficient (ΔF) in the model to describe inbreeding depression was evaluated. Pedigree information from 8,054 animals born between 1976 and 2008 and 4,497 lactation records obtained from 12 herds were used. The realized effective population size was 40.10±1.27, and the mean F of the entire population was 2.14%. The ratio between the number of founders and ancestors demonstrated the existence of a bottleneck in the pedigree of this population, which may contribute to a reduction of genetic diversity. The effect of F on MY, FY, PY, MProd, and SCS was −1.005kg, −0.299kg, −0.246kg, −1.201kg, and −0.002 units, and the effect of ΔF transformed to equivalent F (%) for a mean of 2.57 equivalent generations was −4.287kg, −0.581kg, −0.383kg, −2.001kg, and −0.007 units, respectively. The inbreeding depression observed may have important economic repercussions for production systems. The ΔF can be considered the better of the two indicators of inbreeding depression due to its properties that prevent underestimation of this effect. A designed mating system to avoid inbreeding may be applied to this population to maintain genetic diversity.

Pedigree analysis and inbreeding depression on growth traits in Brazilian Marchigiana and Bonsmara breeds1

The study of population structure by pedigree analysis is useful to identify important circumstances that affect the genetic history of populations. The intensive use of a small number of superior individuals may reduce the genetic diversity of populations. This situation is very common for the beef cattle breeds. Therefore, the objectives of the present study were to analyze the pedigree and possible inbreeding depression on traits of economic interest in the Marchigiana and Bonsmara breeds and to test the inclusion of the individual inbreeding coefficient (F(i)) or individual increases in inbreeding coefficient (ΔF(i)) in the genetic evaluation model for the quantification of inbreeding depression. The complete pedigree file of the Marchigiana breed included 29,411 animals born between 1950 and 2003. For the Bonsmara breed, the pedigree file included 18,695 animals born between 1988 and 2006. Only animals with at least 2 equivalent generations of known pedigree were kept in the analyses of inbreeding effect on birth weight, weaning weight measured at about 205 d, and BW at 14 mo in the Marchigiana breed, and on birth weight, weaning weight, and scrotal circumference measured at 12 mo in the Bonsmara breed. The degree of pedigree knowledge was greater for Marchigiana than for Bonsmara animals. The average generation interval was 7.02 and 3.19 for the Marchigiana and Bonsmara breed, respectively. The average inbreeding coefficient was 1.33% for Marchigiana and 0.26% for Bonsmara. The number of ancestors explaining 50% of the gene pool and effective population size computed via individual increase in coancestry were 13 and 97.79 for Marchigiana and 41 and 54.57 for Bonsmara, respectively. These estimates indicate reduction in genetic variability in both breeds. Inbreeding depression was observed for most of the growth traits. The model including ΔF(i) can be considered more adequate to quantify inbreeding depression. The inclusion of F(i) or ΔF(i) in the genetic evaluation model may not result in better fit to the data. A genetic evaluation with simultaneous estimation of inbreeding depression can be performed in Marchigiana and Bonsmara breeds, providing additional information to producers and breeders.

Effect of the individual coefficients of inbreeding and grading calculated at different ancestral generations of pedigree regarding body proportions of Shagya horses

The objectives of the present study were to investigate the effect of the inbreeding and the rate of genetic plasma from Arabian breed regarding the body proportions in real Shagya population. The analyses of variance of the indexes for bone system development, compactness, massiveness and chest development and estimations of the levels of factors were made by regression, classification and mixed linear models. The individual inbreeding coefficient and grading induced a considerable variance regarding the body proportions during the study. Their use as linear and non-linear regressions or classification factors in the structure of linear models led to a considerably reduction of the rate of an unexplained variance. The nonlinear effect of the inbreeding was statistically proved regarding the chest index at 6-months of age, the massiveness at 1-year of age, and the bone system development and the body compactness at 3-years of age. The grading calculated in the V th and VI th generation of pedigrees was an important source of variation in the late postnatal growth concerning the chest and bone system development. The grading in the IV th generation of pedigrees was significant for a description of the variance of compactness. Synergetic effect was established of the linear and quadratic regressions for the grading calculated in the V th and VI th generation of pedigrees in the chest index. The interactions between the grading from the studied generations of pedigrees were sources of a specific variance regarding the bone system development and the interactions between the grading and inbreeding calculated in the VI th generation of pedigrees induced a variety regarding the massiveness. It was established an increased sensitiveness of the massiveness to higher levels of complex inbreeding increasing the grading.

No inbreeding effects on body size in two captive endangered gazelles

Selection for body size is intricate, involving trade-offs between energy costs, reproductive output, foraging efficiency, and interaction with other community members. In dimorphic, polygynous ungulates, body size is highly correlated with reproductive success in both sexes. Body size has been proposed as a potential phenotypic indicator of genetic change, in wild and in captive populations. We analysed the relationship between adult body size and inbreeding in two captive populations of endangered gazelles. Two estimates of inbreeding were used: individual inbreeding coefficient ( F i ) and individual increase in inbreeding (Δ F i ). Six cranial traits and eight post-cranial bones were measured in 87 Cuvier's gazelles and 97 Mohor gazelles. The average level of individual inbreeding found for the alive population of Cuvier's gazelle was 0.236 and for Mohor gazelle 0.260. Our study demonstrated that within our populations most variability in body size is explained by sex, but we have not found any evidence of inbreeding depression in this morphological trait. Our results are surprising in the light of a widely held belief that from an evolutionary point of view close inbreeding has deleterious effects. The great diversity of factors acting on the effects of inbreeding on trait values make difficult to provide a simple framework to understand them all, hence, we suggest fitness consequences of inbreeding has to be assessed considering the conditions under which one should expect inbreeding depression.

Monogeny, a neglected mechanism of inbreeding avoidance in small populations of gall midges

SeveralspeciesinthefamilyCecidomyiidae(Diptera)areknownbyaparticularreproductionmechanism called monogeny, in which all offspring of each individual female are either exclusively male or exclusively female. As a consequence, no full-sib mating occurs in monogenous populations. So offspringofeach femalemust inevitablymatewiththoseofother females,andintheworst condition, mating may occur between individuals with a common sire but different mothers, where they are only half siblings. Simulation of monogenous gall midge pedigrees, calculation of inbreeding coefficients of individuals for 20 generations, and comparing the results with those of a non-monogenous species revealed that the totalaverageinbreeding coefficients ofindividualswerenot dramatically different between these two populations. However, the maximum inbreeding coefficient of individuals per generation in non-monogenous populations was significantly higher than in monogenous populations. Despite the effect of monogeny on inbreeding, it is doubted whether inbreeding avoidance is theonlyforcethat drivestheevolutionofmonogenyingallmidges.

Population structure of Brazilian Gyr dairy cattle

The objective of the present study was to evaluate the genetic structure of Gyr cattle selected for milk production. Files of pedigree and production were composed of 27,610 animals. The ENDOG program was used for the calculation of individual inbreeding coefficient (F) and coefficient of average relatedness (AR), effective number of animals(Ne), effective number of founders (f e) and ancestors (f a), and generation interval (GI). Individual inbreeding coefficients and average relatedness in the population were 2.82% and 2.10%, respectively. It was observed a reduction in the effective number of animals, especially after publication of the results of the first progeny test. The estimated effective number of founders was 146 and 75 for the ancestrals. Out of those, only 28 ancestors accounted for the origin of 50% of the population genes. The average generation interval was 8.41 years and it was longer for males than for females. For maintaining genetic variability in future generations, it should be invested mating strategies that reduce inbreeding and which do not use massively only some high breeding value sires.

Inbreeding coefficient and heterozygosity-fitness correlations in unhatched and hatched song sparrow nestmates

Heterozygosity-fitness correlations use molecular measures of heterozygosity as proxy estimates of individual inbreeding coefficients (f) to examine relationships between inbreeding and fitness traits. Heterozygosity-fitness correlations partly depend on the assumption that individual heterozygosity and f are strongly and negatively correlated. Although theory predicts that this relationship will be strongest when mean f and variance in f are high, few studies of heterozygosity-fitness correlations include estimates of f based on pedigrees, which allow for more thorough examinations of the relationship between f, heterozygosity and fitness in nature. We examined relationships between pedigree-based estimates of f, multilocus heterozygosity (MLH) and the probability of survival to hatch in song sparrow nestmates. f and MLH were weakly, but significantly negatively correlated. Inbreeding coefficient predicted the probability of survival to hatch. In contrast, MLH did not predict the probability of survival to hatch nor did it account for residual variation in survival to hatch after statistically controlling for the effects of f. These results are consistent with the expectation that heterozygosity-f correlations will be weak when mean and variance in f are low. Our results also provide empirical support for recent simulation studies, which show that variation in MLH among siblings with equal f can be large and may obscure MLH-fitness relationships.

Effect of inbreeding on growth and reproductive traits of Nellore cattle in Brazil

The objective of this study was to identify and quantify the influence of F (inbreeding coefficient) on weaning weight (WW), weight gain from weaning to 18 months of age (WG345), finishing visual score (precocity) at 18 months of age, muscling visual score at 18 months of age (MUS), hip height (HH), scrotal circumference at 18 months of age (SC), heifer probability of pregnancy at 14 months of age (PP14), and stayability (STAY) in Brazilian Nellore cattle. The complete pedigree included 417,552 animals born between 1984 and 2007 on 12 farms located in the states of Mato Grosso do Sul, São Paulo and Bahia. Following the observation of a statistically significant effect ( P < 0.05) of the covariates individual inbreeding coefficient ( F) and maternal inbreeding coefficient, regression analysis of each trait, adjusted for all other effects, was performed as a function of the linear and quadratic effect of F and maternal F (when significant). Inbreeding negatively affected all traits studied ( P < 0.05), except for muscling. A quadratic effect of individual F on WW, WG345, HH and PP14, and a quadratic effect of maternal F on WG345 and HH were observed. Levels of inbreeding higher than 7–11% affected negatively growth and reproductive performance of Nellore cattle. Therefore, inbreeding should be avoided, except for purposes of genetic breeding whose main objective is the fixation of certain alleles in the population.

Improving the estimation of realized effective population sizes in farm animals

Computation of inbreeding rate (DeltaF) must consider that inbreeding is delayed with one generation with respect to the idealized population when addressed using individual inbreeding coefficients. The expression relating inbreeding in generation t with inbreeding rate F(t) = 1 - (1-DeltaF)(t) should be more correctly written in real animal populations as F(t) = 1 - (1-DeltaF)(t-1), as changes in allele frequencies occur in the equivalent co-ancestries in the previous generation. This simple approach is tested on simulated and real pedigrees thus demonstrating that: (i) the adjusted individual increase in inbreeding becomes stable in populations under random mating while the unadjusted parameter does not; (ii) regression of the unadjusted parameter over generations in pedigrees under random mating is highly significant while after correction it is not significant; and (iii) the variance of the adjusted parameter is reduced with the generations.

Role of selection and inbreeding on the incidence of cutaneous malignant melanoma in Sinclair swine

This paper reports the quantitative analysis of the historical database of a herd of Sinclair swine affected by cutaneous malignant melanoma. The herd was under partial and non-systematic selection for melanoma susceptibility (animals having at least one tumour during the first 6 weeks of life). Weighted selection differentials for the number of tumours at birth and the number of tumours at 6 weeks were generally positive and between -0.43 and 4.76 tumours for the number of tumours at 6 weeks. Estimates of the heritability for number of tumours at birth and at 6 weeks using 1934 animals were 0.27 (+/-0.03) and 0.25 (+/-0.03), respectively. The estimate of the genetic correlation between these two traits was 0.95 (+/-0.03). Genetic trends were positive for the number of tumours at birth and at 6 weeks. In spite of positive selection differentials and a moderate heritability, there was a negative phenotypic trend in the number of tumours. Natural selection might be acting in a direction opposite to artificial selection in the Sinclair herd. The slopes of the regression of the number of tumours at birth, at 6 weeks, and melanoma susceptibility on individual inbreeding coefficients were non-significant, indicating no evidence of dominance. The number of live-born pigs was lower in litters from parents susceptible to the disease (p < 0.01).

POPREP: a generic report for population management

Genetic variation provides a basis upon which populations can be genetically improved. Management of animal genetic resources in order to minimize loss of genetic diversity both within and across breeds has recently received attention at different levels, e.g., breed, national and international levels. A major need for sustainable improvement and conservation programs is accurate estimates of population parameters, such as rate of inbreeding and effective population size. A software system (POPREP) is presented that automatically generates a typeset report. Key parameters for population management, such as age structure, generation interval, variance in family size, rate of inbreeding, and effective population size form the core part of this report. The report includes a default text that describes definition, computation and meaning of the various parameters. The report is summarized in two pdf files, named Population Structure and Pedigree Analysis Reports. In addition, results (e.g., individual inbreeding coefficients, rate of inbreeding and effective population size) are stored in comma-separate-values files that are available for further processing. Pedigree data from eight livestock breeds from different species and countries were used to describe the potential of POPREP and to highlight areas for further research.

Inbreeding and testicular abnormalities in a bottlenecked population of koalas (Phascolarctos cinereus)

Habitat destruction and fragmentation, interactions with introduced species or the relocation of animals to form new populations for conservation purposes may result in a multiplication of population bottlenecks. Examples are the translocations of koalas to French Island and its derivative Kangaroo Island population, with both populations established as insurance policies against koala extinction. In terms of population size, these conservation programs were success stories. However, the genetic story could be different. We conducted a genetic investigation of French and Kangaroo Island koalas by using 15 microsatellite markers, 11 of which are described here for the first time. The results confirm very low genetic diversity. French Island koalas have 3.8 alleles per locus and Kangaroo Island koalas 2.4. The present study found a 19% incidence of testicular abnormality in Kangaroo Island animals. Internal relatedness, an individual inbreeding coefficient, was not significantly different in koalas with testicular abnormalities from that in other males, suggesting the condition is not related to recent inbreeding. It could instead result from an unfortunate selection of founder individuals carrying alleles for testicular abnormalities, followed by a subsequent increase in these alleles’ frequencies through genetic drift and small population-related inefficiency of selection. Given the low diversity and possible high prevalence of deleterious alleles, the genetic viability of the population remains uncertain, despite its exponential growth so far. This stands as a warning to other introductions for conservation reasons.

Extra-pair mate choice in the female great tit Parus major: good males or compatible males

The good genes hypothesis and the genetic compatibility hypothesis are the two main hypotheses that focus on the genetic benefit that a female can gain through her choice of a mate. We tested the two hypotheses on extra-pair mating in the great tit, Parus major. We found that female great tits choose males on the basis of breast stripe width, which is in accordance with the good genes hypothesis. Although females chose less related extra-pair males, the evidence for female choice for compatible males was overall weak. However, our data suggest a post-copulatory mechanism of inbreeding avoidance. The observed individual inbreeding coefficient, F, was similar for within-pair offspring (WPO) and extra-pair offspring (EPO). The observed individual F of WPO was lower than the expected individual F, whereas the observed F of EPO was similar to what was expected. These results highlight the importance of processes after copulation for the outcome of female mate choice. Our study shows that in a system with apparent pre-copulatory female choice for good genes, a post-copulatory mechanism may still promote the production of offspring that carry compatible genes.

Assessment of inbreeding depression for body measurements in Spanish Purebred (Andalusian) horses

Our aim was to ascertain inbreeding depression in the Spanish Purebred horses for eight body measurements. A total of 16,472 individuals were measured for height at withers, height at chest, leg length, body length, width of chest, heart girth circumference, knee perimeter and cannon bone circumference. Three different multivariate animal models including, respectively, no measure of inbreeding, individual inbreeding coefficients ( F i ) or individual increase in inbreeding coefficients (Δ F i ) as linear covariates were used. Significant inbreeding depression was assessed. Even though the models including measures of inbreeding fitted better with data, no effect on estimates of genetic parameters was assessed. However, the inclusion of inbreeding measures affected the ranking order according to the Expected Breeding Values (EBV). Due to the better fit with data and nice properties (the adjustment of individual inbreeding coefficients with the pedigree depth and linear behaviour) the use of Δ F i in the evaluation models can be recommended for morphological traits in horses.

Multilocus heterozygosity and inbreeding in the Siberian jay

Because of its common negative association with fitness, inbreeding is a major concern in conservation biology. Traditionally it has been measured as individual inbreeding coefficient calculated from the pedigree, but recently multilocus heterozygosity estimates have become commonly used as proxies. However, theoretical and simulation studies have cast doubt on the validity of these surrogates especially when they are based on only a few molecular markers. Yet, empirical studies reporting the correlation between multilocus heterozygosity and inbreeding coefficient are rare. We studied this relationship in a wild Siberian jay (Perisoreus infaustus) population subject to a long-term field study over 30 years. The correlations between inbreeding coefficient and the employed heterozygosity measures—standardized heterozygosity and internal relatedness—based on 21 microsatellite loci were weak. These results together with results from theoretical and simulation studies caution against use of multilocus heterozygosity estimates to study inbreeding in natural populations.