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Male-male competition magnifies inbreeding depression in wild house mice.

The detrimental effects of inbreeding on vertebrates are well documented for early stages of the life cycle in the laboratory. However, the consequences of inbreeding on long-term survival and reproductive success (Darwinian fitness) are uncertain for vertebrates in the wild. Here, we report direct experimental evidence for vertebrates that competition increases the harmful effects of inbreeding on offspring survival and reproduction. We compared the fitness of inbred (from full-sib matings) and outbred wild house mice (Mus domesticus) in large, seminatural enclosures. Inbred males sired only one-fifth as many surviving offspring as outbred males because of their poor competitive ability and survivorship. In laboratory conditions, inbreeding had relatively minor effects on male reproductive success and no effect on survivorship. Seminatural conditions did not increase inbreeding depression for females, probably because females were not competing for any critical resources. The overall reduction in fitness from inbreeding was 57%, which is 4.5 times as great as previous estimates from the laboratory. These results have important implications for medicine, conservation, evolutionary biology, and functional genomics.

Animals↗

Inbreeding and heterosis effects on quantitative traits in a White Leghorn population under long-term reciprocal recurrent selection.

1. Inbreeding and heterosis effects for quantitative traits were estimated in two White Leghorn lines selected with reciprocal recurrent selection (RRS) since 1950. 2. Pedigreed progeny were produced from full-sib, half-sib and unrelated pure line as well as reciprocal cross line matings to estimate inbreeding and heterosis effects "within sires". 3. Inbreeding effects estimated as linear regressions agreed well with estimates considering inbreeding as fixed effect. The inbreeding depression per 10% inbreeding was highest for hatchability (6-7%), intermediate for production-related traits (3%), and about 1% for shell quality, body weight and egg weight. 4. Heterosis effects were estimated by comparing pure line and cross line progeny of the same sires. 5. Results indicate considerably less heterosis for egg production than found earlier, which is interpreted as a consequence of pure line selection.

Animals↗

Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster.

The rate of decline in reproductive fitness in populations of Drosophila melanogaster inbred at an initial rate of approximately 1% per generation has been investigated under both competitive and noncompetitive conditions. Breeding population size was variable in the inbred lines with an estimated harmonic mean of 66.7 +/- 2.2. Of the 60 lines maintained without reserves, 75% survived a period of 210 generations of slow inbreeding and were then rapidly inbred by full-sib mating to near-homozygosity. The initial rate of inbreeding was estimated to be 0.96 +/- 0.16% per generation, corresponding to an effective population size of approximately 50. However, the rate of inbreeding declined significantly with time to average only 0.52 +/- 0.08% per generation over the 210 generation period, most likely due to associative overdominance built up by genetic sampling and selection in the small populations. The total inbreeding depression in fitness was estimated to be 87 +/- 3% for competitive ability and 27 +/- 5% for fitness under uncrowded conditions, corresponding to rates of decline of 2.0 +/- 0.3 and 0.32 +/- 0.07%, respectively, per 1% increase in the inbreeding coefficient. The frequency of lethal second chromosomes in the resultant near-homozygous lines was of the order of 5%, lethal free second chromosomes showed a mean viability under both crowded and uncrowded conditions of approximately 95%, and their population cage fitness was 60% that of Cy/+ heterozygotes. It can be concluded that homozygous genotypes from which deleterious genes of major effect have been eliminated during slow inbreeding may show far less depression in reproductive fitness than suggested by earlier studies of wild chromosome homozygotes. The loss in fitness due to homozygosity throughout the entire genome may be as little as 85-90% under competitive conditions, and 25-30% in an optimal environment.

Animals↗

Fixed contributions designs vs. minimization of global coancestry to control inbreeding in small populations.

Populations with small census sizes are at risk because of the loss of genetic variability and the increase of inbreeding and its harmful consequences. For situations with different numbers of males and females, several hierarchical designs have been proposed to control inbreeding through the fixation of individuals' contributions. An alternative method, based on the minimization of global coancestry, has been proposed to determine contributions as to yield of the lowest levels of inbreeding in the population. We use computer simulations to assess the relative efficiency of the different methods. The results show that minimizing the global coancestry leads to equal or lower levels of inbreeding in the short and medium term, although one of the hierarchical designs provides lower asymptotic inbreeding rates and, thus, less net inbreeding in the long term. We also investigate the performance of the alternative methods against departures from the ideal conditions, such as inbred or differentially related base individuals and random failures in the expected contributions. The method of minimization of global coancestry turns out to be more flexible and robust under these realistic situations.

Conservation of Natural Resources↗

Inbreeding and reproductive performance in standardbred horses.

The relationship between inbreeding and both conception and foaling rates in Standardbred horses (trotters and pacers) was examined for 1194 breeding years. There was a statistically significant (P less than 0.05) trend for conception and foaling rates to decrease with increased inbreeding; however, this relationship accounted for less than 2 percent of the variation. Additionally, the relationship between reproductive performance and inbreeding was not consistent between trotters and pacers. For trotters (F = 0.103) there was a trend for an increase in conception and foaling rates with increased inbreeding, while for pacers (F = 0.074), reproductive performance decreased with increased inbreeding. Overall, inbreeding does not appear to be a significant factor influencing reproductive performance of Standardbred horses.

Animals↗

Inbreeding depression and genetic load in laboratory metapopulations of the butterfly Bicyclus anynana.

We investigated the effects of inbreeding on various fitness components and their genetic load in laboratory metapopulations of the butterfly Bicyclus anynana. Six metapopulations each consisted of four subpopulations with breeding population sizes of N = 6 or N = 12 and migration rate of m = 0 or m = 0.33. Metapopulations were maintained for seven generations during which coancestries and pedigrees were established. Individual inbreeding coefficients at the F7 were calculated and ranged between 0.01 and 0.51. Even though considerable purging had occurred during inbreeding, the genetic load remained higher than that of many outbreeding species: approximately two lethal equivalents were detected for egg sterility, one for zygote survival, one for juvenile survival, and one for longevity. Severe inbreeding depression occurred after seven generations of inbreeding, which jeopardized the metapopulation survival. This finding suggests that the purging of genetic load by intentional inbreeding cannot be recommended for the genetic conservation of species with a high number of lethal equivalents.

Animals↗

The cost of fluctuating inbreeding depression.

We present a phenotypic model for the evolution of self-fertilization in an infinite population of annual hermaphrodites for the case in which fitness and inbreeding depression vary among generations (e.g., due to fluctuations in the environment from year to year). Conditions for the evolution of selfing, mixed mating, and outcrossing are derived and are compared with results from numerical calculations that assume a normal distribution of inbreeding depression. In contrast to the situation in which inbreeding depression does not vary, when inbreeding depression fluctuates in a stochastic manner among generations with a mean less than 0.5, selfing is not necessarily selected. Thus, fluctuating inbreeding depression can be viewed as an additional cost of selfing that may stabilize mixed mating systems. These results emphasize the need to take into account fluctuating inbreeding depression in empirical studies aimed at understanding mating system evolution in annuals.

Biological Evolution↗

Genetic and functional evaluation of the level of inbreeding of the Westran pig: a herd with potential for use in xenotransplantation.

BACKGROUND: The Westran pig has been purposely inbred for use in xenotransplantation. The herd originated in the wild from a limited gene pool and has been inbred by repeated full-sib matings for nine generations. METHODS: The aim of this study was to evaluate the level of inbreeding by functional assays, such as bi-directional MLR and reciprocal skin grafts between herd members, and by genetic analysis using highly polymorphic genetic markers to calculate the level of inbreeding. RESULTS: The MLR between herd members were non-reactive whereas there was a prompt response to third party pig lymphocytes, indicative of a normal immune responsiveness in Westran pigs but isogenicity of the major histocompatibility complex. Skin grafts between male siblings or female sibling skin grafts on male recipients showed prolonged survival but with few exceptions did not survive beyond 100 days suggesting that by the fifth generation the Westran herd was still mismatched at minor histocompatibility antigens. This level of functional inbreeding was confirmed by microsatellite analysis of highly polymorphic markers, which showed that 52 of 53 chromosomally dispersed markers were fixed by the ninth generation. This level of fixation was consistent with 19 to 20 generations of full-sibling inbreeding. The calculated inbreeding coefficient at generation 10 was 0.98159. CONCLUSIONS: This analysis confirms that the Westran pig is highly inbred and we propose that analysis of chromosomally dispersed highly polymorphic markers is an accurate and reproducible method for assessing the level of inbreeding of a pig herd.

Aging↗

Does inbreeding avoidance maintain gender dimorphism in Wurmbea dioica (Colchicaceae)?

The maintenance of females in gender dimorphic populations requires that they have a fitness advantage to compensate for their loss of male reproductive function. We assess whether inbreeding avoidance provides this advantage in two subdioecious Wurmbea dioica populations by estimating seed production, outcrossing rates and inbreeding depression. Fruiting males produced less than half as many seeds as females, owing to low outcrossing rates and early acting inbreeding depression. Inbreeding coefficients of fruiting males demonstrated that progeny were more inbred than their parents, implying that few selfed progeny reach maturity, as confirmed by inbreeding depression estimates that exceeded 0.85. In a glasshouse experiment, open-pollinated females exhibited a fitness advantage of 3.7 relative to fruiting males, but when we increased fruiting male outcrossing rate, female advantage was only 1.4. This reduced advantage is insufficient to maintain females if nuclear genes control sex. Thus, inbreeding avoidance could maintain females at high frequencies, although this is contingent upon high frequencies of fruiting males, which can be altered by environmentally determined gender plasticity.

Biological Evolution↗

Prediction of inbreeding in commercial females maintained by rotational mating with partially isolated sire lines.

The solution to the inbreeding problem for livestock breeds in commercial use is often complicated by hierarchical population structure, in which favourable genes are accumulated in the upper level of the hierarchy (breeding population) by artificial selection and the genetic progress achieved is transferred to the lower level through migration of males. When the breeding population is subdivided into several isolated lines, rotational mating with the lines has been shown to be quite an effective system to reduce the short- and long-term inbreeding of commercial females in the lower level. In practice, however, some amount of migration should be allowed among the lines to reduce the rate of inbreeding in each line. In this study, we developed the recurrence equation for the inbreeding coefficient of the commercial females maintained by the rotational mating with partially isolated lines. Numerical computations were carried out to evaluate the effect of the migration on the efficiency of the rotational mating. It was shown that even with a small amount of migration among the lines, the inbreeding of commercial females is substantially inflated. However, when four or five lines are available, the inbreeding coefficient of commercial females can be suppressed to an acceptable level, irrespective of the effective size of line and the migration rate. Application of the mating system to the population of Japanese Black cattle was also examined.

Animals↗

Pollinator limitation and inbreeding depression in orchid species with and without nectar rewards.

Many orchids produce no nectar rewards. Foraging pollinators should visit more flowers per inflorescence in species with nectar, which could increase geitonogamous self-fertilization. If a history of selfing decreases genetic load, then nectar-producing orchids should harbour lower inbreeding depression than nectarless species. Here, I tested this hypothesis by quantifying inbreeding depression and pollinator limitation in populations of three closely related orchid species, one of which provides nectar. I also compared inbreeding depression for nectarless and nectar-producing species of orchids using published studies. All field populations expressed pollinator limitation, but the nectar-providing species was intermediate to the two nectarless species. All populations expressed inbreeding depression, and levels increased in later life-history stages. There was no tendency for nectarless species to express higher inbreeding depression either in experiments or published studies. Nectarless orchids may not express higher levels of inbreeding depression because pollinators fail to visit more flowers in nectar-bearing species, because such visitations do not result in greater selfing, and/or because higher selfing may be ineffective in purging the mutations that cause load.

Ecosystem↗

Reduction of inbreeding in commercial females by rotational mating with several sire lines.

A mating system to reduce the inbreeding of commercial females in the lower level was examined theoretically, assuming a hierarchical breed structure, in which favorable genes are accumulated in the upper level by artificial selection and the achieved genetic progress is transferred to the lower level through migration of males. The mating system examined was rotational mating with several closed sire lines in the upper level. Using the group coancestry theory, we derived recurrence equations for the inbreeding coefficient of the commercial females. The asymptotic inbreeding coefficient was also derived. Numerical computations showed that the critical factor for determining the inbreeding is the number of sire lines, and that the size of each sire line has a marginal effect. If four or five sire lines were available, rotational mating was found to be quite an effective system to reduce the short- and long-term inbreeding of the commercial females, irrespective of the effective size of each sire line. Oscillation of the inbreeding coefficient under rotational mating with initially related sire lines could be minimized by avoiding the consecutive use of highly related lines. Extensions and perspectives of the system are discussed in relation to practical application.

Animals↗

Inbreeding depression and male survivorship in Drosophila: implications for senescence theory.

The extent to which inbreeding depression affects longevity and patterns of survivorship is an important issue from several research perspectives, including evolutionary biology, conservation biology, and the genetic analysis of quantitative traits. However, few previous inbreeding depression studies have considered longevity as a focal life-history trait. We maintained laboratory populations of Drosophila melanogaster at census population sizes of 2 and 10 male-female pairs for up to 66 generations and performed repeated assays of male survivorship throughout this time period. On average, significant levels of inbreeding depression were observed for median life span and age-specific mortality. For age-specific mortality, the severity of inbreeding depression increased over the life span. We found that a baseline inbreeding load of 0.307 lethal equivalents per gamete affected age-specific mortality, and that this value increased at a rate of 0.046 per day of the life span. With respect to some survivorship parameters, the differentiation of lineages was nonlinear with respect to the inbreeding coefficient, which suggested that nonadditive genetic variation contributed to variation among lineages. These findings provide insights into the genetic basis of longevity as a quantitative trait and have implications regarding the mutation-accumulation evolutionary explanation of senescence.

Animals↗

Maximizing the response of selection with a predefined rate of inbreeding.

A method was derived that maximizes the genetic level of selected animals while constraining their average coancestry to a predefined value. The average coancestry of the selected parents equals the inbreeding level in the next generation, so that rates of inbreeding were controlled. When this method was applied for several generations of selection, stable rates of genetic gain were attained, which indicates that the method could control the short- and long-term effects of selection on inbreeding. At equal rates of inbreeding, genetic gains were 21 to 60% greater than that with selection for BLUP-EBV, because of increased selection differentials. The difference was larger when the desirable rate of inbreeding was smallest. Selection with a constraint on inbreeding required only EBV of, and relationships between, the selection candidates and is therefore easy to apply in practice. The optimal solution is expressed in genetic contributions of selection candidates to the next generation, which is equivalent to numbers of offspring per candidate. These optimal numbers of offspring may be difficult to attain because of female reproductive limitations. The optimal method could be adapted to situations with additional reproductive constraints. The method can also be used to constrain the variance of response by restricting the average prediction error variance of the selected animals.

Animal Husbandry↗

Maximizing the response of selection with a predefined rate of inbreeding: overlapping generations.

In a breeding scheme, the aim is high rates of genetic gain with limited inbreeding. A dynamic selection rule is developed that maximizes selection response in populations with overlapping generations. The rule maximizes the genetic merit of selected animals while limiting the average relationship of the population after the current round of selection. The latter is shown to limit the contribution of the current population to the future inbreeding. The rule accounts for the selection of some candidates during previous selection rounds and for the expected future contributions of the selection candidates. Inputs for the rule are the BLUP breeding values and ages of selection candidates, the relationship matrix of all animals, and contributions of animals during previous selection rounds. Output is the optimal number of offspring for each candidate. Computer simulations of dairy cattle nucleus schemes showed that predefined rates of inbreeding were actually achieved, without compromising long-term selection response, at least up to 20 yr of selection. At the same rates of inbreeding, the dynamic selection rule obtained up to 44% more genetic gain than direct selection for BLUP breeding values. The advantage of the dynamic rule over BLUP selection decreased with increasing population sizes and with greater predefined rates of inbreeding. Consequently, the dynamic rule should be especially useful in small selection schemes in which relatively low rates of inbreeding are desired.

Age Factors↗

Effects of mild inbreeding on productive and reproductive performance of Guernsey cattle.

Production and reproduction records that spanned a 24-yr period were used to study the effects of low coefficients of inbreeding in two experiment station Guernsey herds. Inbreeding ranged from 0 to 25.3% and averaged 4.1%. Milk and fat yields were all first lactations standardized to a mature equivalent, twice daily milking, and 305 d. Intrasire regressions of production traits on percent inbreeding were -23.8 kg of milk, -1.25 kg of fat, and .002% for fat percentage. Estimates of the effect of inbreeding on reproductive traits had large standard errors but suggested that inbreeding depressed reproductive performance. Age at first calving decreased 3.7 d per 1% increase in inbreeding.

Animals↗

Inbreeding of and relationship among registered Holsteins.

Holstein-Friesian Herdbooks (Holstein-Friesian Association of America, Brattleboro, VT) were used to draw random samples of 600 registered females born during each of the yr 1970, 1976, and 1982. A two-line pedigree, one random line of ancestry tracing from the sire and another tracing from the dam to the beginning of the Holstein-Friesian Herdbook, was tabulated for each of these 1800 females. These were used to estimate inbreeding and inter se relationship for the Holstein breed. Estimates of inbreeding were 4.7, 3.8, and 4.3% for 1970, 1976, and 1982. These estimates were not different from one another or from 1928 and 1931 estimates. Estimates of inter se relationship were 5.2, 7.3, and 9.8% for 1970, 1976, and 1982. These estimates were different from one another and from an estimate of 3.4% for 1931. The increase in inter se relationship without corresponding increase in inbreeding indicates that a change in mating strategies has evolved over time. The majority of breeders now apparently mate animals that are less related than if mating was random, whereas in the past there was more of a tendency to mate within the same line. Despite these attempts to avoid inbreeding, it may be only a matter of time until increasing inter se relationship causes an increase in inbreeding. Because of detrimental effects associated with inbreeding, it is important that the Holstein breed be monitored on a regular basis for these parameters. Ancestors that occurred most frequently in the 1982 sample were identified and their direct relationships to the breed tabulated for the years studied.

Animals↗

Nonadditive genetic effects and inbreeding depression for somatic cell counts of Holstein cattle.

A total of 65,491 lactation means of log2-transformed SCC measures were analyzed from first lactation Holstein cows in Ontario. Effects of inbreeding on SCC were estimated by a nonadditive sire and dam model that included additive, dominance, and additive by additive genetic effects and regression of lactation somatic cell score on inbreeding coefficients of the cows. Variance components were estimated using the tildehat approximation to REML. Solutions were by iteration on data. Estimates of heritability for lactation somatic cell score in the narrow sense were .165 and in the broad sense were .203. The additive by additive component (2.5% of the total phenotypic variance) was almost twice as large as the dominance component (1.3%). The regression coefficient of lactation somatic cell score per 1% increase of inbreeding was .012. The average increase of the population mean of lactation somatic cell score caused by a 10% increase of inbreeding coefficient was estimated to be 10.5% of the original phenotypic standard deviation of 1.153. The inbreeding depression was thus relatively low, but, on average, inbred animals tended to have higher lactation somatic cell score. This study provides preliminary evidence that inbreeding is related to disease prevalence in large purebred dairy populations.

Animals↗