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Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae).

Owing to habitat loss populations of many organisms have declined and become fragmented. Vertebrate conservation strategies routinely consider genetic factors, but their importance in invertebrate populations is poorly understood. Bumblebees are important pollinators, and many species have undergone dramatic declines. As monoandrous social hymenopterans they may be particularly susceptible to inbreeding due to low effective population sizes. We study fragmented populations of a bumblebee species, on a model island system, and on mainland Great Britain where it is rare and declining. We use microsatellites to study: population genetic structuring and gene flow; the relationships between genetic diversity, population size and isolation; and frequencies of (sterile) diploid males - an indicator of inbreeding. We find significant genetic structuring (theta = 0.12) and isolation by distance. Populations > 10 km apart are all significantly differentiated, both on oceanic islands and on the mainland. Genetic diversity is reduced relative to closely related common species, and isolated populations exhibit further reductions. Of 16 populations, 10 show recent bottlenecking, and 3 show diploid male production. These results suggest that surviving populations of this rare insect suffer from inbreeding as a result of geographical isolation. Implications for the conservation of social hymenopterans are discussed.

Animals↗

A fast algorithm for computing inbreeding coefficients in large populations.

Inbreeding coefficients of animals are required in many genetic analyses of livestock records. A modification of Colleau's indirect algorithm to compute inbreeding coefficients in large populations is presented. With overlapping generations, the modified algorithm evaluated all progeny of each sire simultaneously in one back and forth exploration of a reduced pedigree. Simulation for a relatively large number of generations, different number of sires, family sizes and mating designs showed that Colleau's algorithm was faster (from 1.2 to 143 times) than two other algorithms under comparison (Tier, modified Meuwissen and Luo), in all situations investigated. Modifying Colleau's algorithm considerably decreased computation time (from 50 to 89%), resulting in a very fast algorithm. The number of sires mostly affected computational efficiency of the modified algorithm, whereas family size and mating design had virtually no effect. In the updating situation, when only animals born in the last year were evaluated, given known inbreeding coefficients for the other, the modified algorithm was also fast compared with the other three algorithms. Memory requirements for the algorithms were also discussed.

Algorithms↗

Pedigree information reveals moderate to high levels of inbreeding and a weak population structure in the endangered Catalonian donkey breed.

The Catalonian donkey is one of the most endangered donkey breeds in the world. At present, five main subpopulations exist: AFRAC, which consists of many genetically connected Catalonian localities; Berga, which consists of a single herd located also in Catalunya but under private management; and three minor non-Catalonian subpopulations (Huesca, Sevilla and Toledo). In this study, we analysed the pedigree information of the Catalonian donkey herdbook to assess the genetic diversity and population structure of the breed. We found that the Catalonian donkey has suffered an important loss of genetic diversity and moderate to high increases of inbreeding because of the abuse of a few individuals in matings. This scenario is mainly characterized by the fact that both the effective number of founders and ancestors for the whole population was 70.6 and 27, respectively, while the equivalent number of founders was 146.5 and the number of ancestors explaining overall genetic variability was 93. In addition, only 14% of animals born between the 1960s and 1970s were significantly represented in the pedigree. Our results also show that subpopulations where breeders exchanged reproductive individuals had low levels of inbreeding and average relatedness. One subpopulation, Berga, was reproductively isolated and showed high levels of inbreeding (F = 7.22%), with average relatedness (AR = 6.61%) playing an important role in increasing the values of these coefficients in the whole pedigree. Using genealogical F-statistics we have found little evidence of population structuring (F(ST) = 0.0083) with major genetic differences among non-Catalonian subpopulations.

Animals↗

Inbreeding effects on progeny sex ratio and gender variation in the gynodioecious Silene vulgaris (Caryophyllaceae).

In gynodioecious species, sex expression is generally determined through cytoplasmic male sterility genes interacting with nuclear restorers of the male function. With dominant restorers, there may be an excess of females in the progeny of self-fertilized compared with cross-fertilized hermaphrodites. Moreover, the effect of inbreeding on late stages of the life cycle remains poorly explored. Here, we used hermaphrodites of the gynodioecious Silene vulgaris originating from three populations located in different valleys in the Alps to investigate the effects of two generations of self- and cross-fertilization on sex ratio and gender variation. We detected an increase in females in the progeny of selfed compared with outcrossed hermaphrodites and inbreeding depression for female and male fertility. Male fertility correlated positively with sex ratio differences between outbred and inbred progeny, suggesting that dominant restorers are likely to influence male fertility qualitatively and quantitatively in S. vulgaris. We argue that the excess of females in the progeny of selfed compared with outcrossed hermaphrodites and inbreeding depression for gamete production may contribute to the maintenance of females in gynodioecious populations of S. vulgaris because purging of the genetic load is less likely to occur.

Disorders of Sex Development↗

Polymorphism in an inbreeding population under models involving underdominance.

Models of selection favoring homozygotes over the heterozygotes and involving frequency-dependency in their competitive abilities were simulated in order to determine the conditions for maintaining stable polymorphism at a diallelic locus in large inbreeding populations. With heavier inbreeding, frequency-dependency could increasingly override the effects of underdominance in both pure stand and the competing ability components of fitness in terms of yielding stable nontrivial equilibriums. The significance of such selection models is discussed for the retention of variability in inbreeding populations with a minimum of segregational load and higher overall stability in contrast to the overdominance models.

Genes, Dominant↗

Joint effects of self-fertilization and population structure on mutation load, inbreeding depression and heterosis.

Both the spatial distribution of organisms and their mode of reproduction have important effects on the change in allele frequencies within populations. In this article, we study the combined effect of population structure and the rate of partial selfing of organisms on the efficiency of selection against recurrent deleterious mutations. Assuming an island model of population structure and weak selection, we express the mutation load, the within- and between-deme inbreeding depression, and heterosis as functions of the frequency of deleterious mutants in the metapopulation; we then use a diffusion model to calculate an expression for the equilibrium probability distribution of this frequency of deleterious mutants. This allows us to derive approximations for the average mutant frequency, mutation load, inbreeding depression, and heterosis, the simplest ones being Equations 35-39 in the text. We find that population structure can help to purge recessive deleterious mutations and reduce the load for some parameter values (in particular when the dominance coefficient of these mutations is <0.2-0.3), but that this effect is reversed when the selfing rate is above a given value. Conversely, within-deme inbreeding depression always decreases, while heterosis always increases, with the degree of population subdivision, for all selfing rates.

Crosses, Genetic↗

Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare.

In human genetics a detailed knowledge of linkage disequilibrium (LD) is considered a prerequisite for effective population-based, high-resolution gene mapping and cloning. Similar opportunities exist for plants; however, differences in breeding system and population history need to be considered. Here we report a detailed study of localized LD in different populations of an inbreeding crop species. We measured LD between and within four gene loci within the region surrounding the hardness locus in three different gene pools of barley (Hordeum vulgare). We demonstrate that LD extends to at least 212 kb in elite barley cultivars but is rapidly eroded in related inbreeding ancestral populations. Our results indicate that haplotype-based sequence analysis in multiple populations will provide new opportunities to adjust the resolution of association studies in inbreeding crop species.

Chromosomes, Plant↗

Joint evolution of dispersal and inbreeding load.

Inbreeding avoidance is often invoked to explain observed patterns of dispersal, and theoretical models indeed point to a possibly important role. However, while inbreeding load is usually assumed constant in these models, it is actually bound to vary dynamically under the combined influences of mutation, drift, and selection and thus to evolve jointly with dispersal. Here we report the results of individual-based stochastic simulations allowing such a joint evolution. We show that strongly deleterious mutations should play no significant role, owing to the low genomic mutation rate for such mutations. Mildly deleterious mutations, by contrast, may create enough heterosis to affect the evolution of dispersal as an inbreeding-avoidance mechanism, but only provided that they are also strongly recessive. If slightly recessive, they will spread among demes and accumulate at the metapopulation level, thus contributing to mutational load, but not to heterosis. The resulting loss of viability may then combine with demographic stochasticity to promote population fluctuations, which foster indirect incentives for dispersal. Our simulations suggest that, under biologically realistic parameter values, deleterious mutations have a limited impact on the evolution of dispersal, which on average exceeds by only one-third the values expected from kin-competition avoidance.

Animals↗

Inbreeding by environmental interactions affect gene expression in Drosophila melanogaster.

Genomewide gene expression patterns were investigated in inbred and noninbred Drosophila melanogaster lines under benign and stressful (high temperature) environmental conditions in a highly replicated experiment using Affymetrix gene chips. We found that both heat-shock protein and metabolism genes are strongly affected by temperature stress and that genes involved in metabolism are differentially expressed in inbred compared with noninbred lines, and that this effect is accentuated after heat stress exposure. Furthermore we show that inbreeding and temperature stress cause increased between-line variance in gene expression patterns. We conclude that inbreeding and environmental stress both independently and synergistically affect gene expression patterns. Interactions between inbreeding and the environment are often observed at the phenotypic level and our results reveal some of the genes that are involved at the individual gene level. Our observation of several metabolism genes being differentially expressed in inbred lines and more so after exposure to temperature stress, together with lower fitness in the investigated inbred lines, supports the hypothesis that superiority of heterozygous individuals partly derives from increased metabolic efficiency.

Animals↗

Predicting rates of inbreeding for livestock improvement schemes.

This article presents a deterministic method to predict rates of inbreeding (deltaF) for typical livestock improvement schemes. The method is based on a recently developed general theory to predict rates of inbreeding, which uses the concept of long-term genetic contributions. A typical livestock breeding population was modeled, with overlapping generations, BLUP selection, and progeny testing of male selection candidates. Two types of selection were practiced: animals were either selected by truncation on estimated breeding values (EBV) across age classes, or the number of parents selected from each age class was set to a fixed value and truncation selection was practiced within age classes. Bulmer's equilibrium genetic parameters were obtained by iterating on a pseudo-BLUP selection index and deltaF was predicted for the equilibrium situation. Predictions were substantially more accurate than predictions from other available methods, which ignore the effect of selection on deltaF. Predictions were accurate for schemes with up to 20 sires. Predicted deltaF was somewhat too low for schemes with more than 20 sires, which was due to the use of simple linear models to predict genetic contributions. The present method provides a computationally feasible (i.e., deterministic) tool to consider both the rate of inbreeding and the rate of genetic gain when optimizing livestock improvement schemes.

Animals↗

Inbreeding and immunoglobulin G1 concentrations in cattle.

Immunoglobulin G1 concentration (IgG1) was measured in presuckle colostrum and calf serum obtained at 36 h and at weaning from inbred and straightbred Angus, Brangus, Hereford, Red Angus and Simmental cattle. Sources of variation considered as dam traits examined for IgG1 in colostrum and 36-h calf serum included line of sire, sire within line, age, and linear regression of IgG1 on inbreeding of dam. Only line of sire and inbreeding of dam were significant in the analysis of 36-h calf serum. Sources of variation considered as calf traits examined for IgG1 in calf serum at 36 h and at weaning included line of sire, sire within line, sex of calf, age of dam, and regressions of calf serum IgG1 on inbreeding of the calf and on dam's colostral IgG1. Only sire within line and the regression on dam's colostral IgG1 were significant for calf serum IgG1 at 36 h. Large differences existed in 36-h calf serum IgG1 between sires both within lines and when lines were ignored. Calves with 36-h serum IgG1 of less than 10 mg/ml were two to four times more likely to die before weaning than calves with higher IgG1 levels. The heritability estimates of IgG1 by paternal half-sib analysis were .41 +/- .30 for colostrum measured as a trait of the dam and .56 +/- .25 for 36-h. calf serum and .05 +/- .17 for calf serum at weaning considered as a trait of the calf. These estimates indicate that IgG1 in colostrum and 36-h calf serum could be increased by selection.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Proven and young Holstein bulls compared for daughter yields, productive life, somatic cell score, and inbreeding.

The objective of this study was to compare daughters of proven (progeny-tested) and young sampling bulls available for use at the same time for yield traits, productive life, somatic cell score, and inbreeding. Data were from USDA sire evaluations of July 1989 through July 1994. Proven bulls used between 1989 and 1994 were identified based on the change in number of daughters. Young bulls were identified based on age and date a bull first entered artificial insemination. Young bulls were classified into two categories: one included all young bulls available in one year and the other included the top 50% on parent average for milk. Daughter deviations for yields, productive life and somatic cell scores, and average inbreeding were obtained from May 2000 evaluation. Daughter deviation milk was not different between proven and top 50% young bulls but was lower for all young bulls. Young bulls (all and top 50%) exceeded proven bulls in daughter deviation fat and protein. Progeny of proven bulls had favorably higher productive life in most years but unfavorably higher somatic cell score than progeny of young bulls. Inbreeding was consistently higher for daughters of young bulls than for those of proven bulls. Results indicate that young bulls were competitive with proven bulls. Use of young bulls from among the top 50% should result in equal or higher genetic progress in yields compared to contemporaries by proven bulls.

Age Factors↗

Inbreeding in Danish dairy cattle breeds.

The purpose of this study was to monitor current and predict future rates of inbreeding in the Danish dairy breeds. Calves born from 1999 until 2003 and registered as Danish Holstein (1,883,983), Danish Jersey (336,966), or Danish Red (261,047) were reference populations. Average complete generation equivalent was approximately 7. For calves born in 2003, average inbreeding was 3.9, 3.4, and 1.4% for Holstein, Jersey, and Danish Red, respectively. In recent years, effective population sizes were 49, 53, and 47, respectively. Based on coancestry statistics, future effective population sizes will be 43, 42, and 51, respectively. The effective number of founders, effective number of ancestors, and effective number of founder genomes were calculated. These measures of genetic diversity were all low for Holstein and Jersey and somewhat larger for Danish Red. The most important ancestors of Danish Holstein were Elevation (13.8%), Chief (10.9%), and Bell (8.5%). The most important ancestor of Danish Red was Momentum (9.4%), a Red Holstein-Friesian. The most important ancestor for Danish Jersey was FYN Lemvig (12.1%) with a large number of progeny in the reference population. The results of this study indicate the necessity for active management of the rate of inbreeding in the future.

Animals↗

Effects of nonadditive genetic interactions, inbreeding, and recessive defects on embryo and fetal loss by seventy days.

Lethal recessive genes that cause early embryo loss are difficult to detect. Nonreturn rate at 70 d after first insemination (NR) was evaluated as a trait of the embryo using 1,739,055 first-service records from 1,251 Holstein bulls represented as both service sires and sires of cows. Effects modeled included herd-year-season, parity of cow, sire of cow, service bull, interaction of service bull with sire of cow, and regression on inbreeding of embryo. Variances of service bull and sire of cow were estimated using REML and estimated effects were removed from the data. Interaction variance was estimated from the residuals using the tilde-hat approximation to REML. An additive relationship matrix was used for sire of cow and a dominance relationship matrix for the interaction term. Service bull effects were assumed constant across time and unrelated. For each 10% increase in inbreeding, NR percentage declined by an estimated 1%. A regression of this size could be explained by > 20% of animals carrying defects that cause early embryo loss. Of the total variance, service bull contributed 0.36%; sire of cow, 0.24% (heritability of 1.0%); and interaction, 0.18% (dominance variance of 2.8%). Numbers of records exceeded 500 for 50 bull pair subclasses. Predicted interactions that included effects of inbreeding ranged from - 3.6% to +2.9%, compared with the mean NR of 56%. The largest negative interactions were not caused by known recessive defects. Complex vertebral malformation generally causes loss of pregnancies later in gestation, and few current bulls carry the gene for deficiency of uridine monophosphate synthase. Further study of the families with largest negative interactions could uncover new recessive defects.

Abortion, Veterinary↗

[Analysis of genealogical structure of populations. II. The use od numerical pedigrees for calculation of inbreeding coefficient].

A method for calculation of inbreeding coefficient F in a numerical pedigree with no reference to its graphic representation is suggested. For calculation of F, a formula that does not take into account inbreeding coefficients of common ancestors and admits intersections in a loop is used. An advantage of this method is that it automatically finds all loops formed by paths to common ancestors. Detecting these loops via their tracing in a graphic pedigree with intersecting lines of descent creates a possibility of errors. A criterion of existence of at least one common link for two numerical paths is presented. It enables one to exclude pairs of paths to common ancestors that do not form loops. The methods considered for computing F in a given pedigree give exact values of the inbreeding coefficient for autosomal and sex-linked loci and generalize the known approximate approaches. The methods are illustrated by examples.

Female↗

Modelling the evolution of female choice strategies under inbreeding conditions.

Recently, many mate choice studies have discussed the role of genetic compatibility and inbreeding for the evolution of mate choice. With population genetic simulations I compared the potential advantage of three different female choice strategies under inbreeding conditions. Females were assumed to benefit indirectly via a preference for (i) complementary males, (ii) males with few detrimental mutations, and (iii) non-inbred males. Probably related to the reduced inbreeding depression in offspring of choosy females, the choice-allele increased for all three strategies. However, the advantage of the strategies differed widely. Choice of males with fewer mutations provided a comparatively large advantage, choice of complementary males led to a reasonable advantage, and choice of non-inbred males only resulted in a minor advantage of female choice. My results show that complementary mate choice can be almost as beneficial as conventional good-genes choice of mates with lower genetic load. Compared to the two other mate choice strategies, choice of non-inbred males is less likely to contribute to the evolution of costly mate choice. The results of a recent study showing that female sticklebacks prefer males with a larger number of MHC-loci is thus unlikely to be related to an indirect benefit of choosing non-inbred males.

Animals↗

Loss of gametophytic self-incompatibility with evolution of inbreeding depression.

Gametophytic self-incompatibility (SI) in plants is a widespread mechanism preventing self-fertilization and the ensuing inbreeding depression, but it often evolves to self-compatibility. We analyze genetic mechanisms for the breakdown of gametophytic SI, incorporating a dynamic model for the evolution of inbreeding depression allowing for partial purging of nearly recessive lethal mutations by selfing, and accounting for pollen limitation and sheltered load linked to the S-locus. We consider two mechanisms for the breakdown of gametophytic SI: a nonfunctional S-allele and an unlinked modifier locus that inactivates the S-locus. We show that, under a wide range of conditions, self-compatible alleles can invade a self-incompatible population. Conditions for invasion are always less stringent for a nonfunctional S-allele than for a modifier locus. The spread of self-compatible genotypes is favored by extremely high or low selfing rates, a small number of S-alleles, and pollen limitation. Observed parameter values suggest that the maintenance of gametophytic SI is caused by a combination of high inbreeding depression in self-incompatible populations coupled with intermediate selfing rates of the self-compatible genotypes and sheltered load linked to the S-locus.

Alleles↗

Inbreeding and relationship in Polish Black-and-White sires.

The aim of the study was to analyse inbreeding and relationship in the Polish population of Black-and-White sires. Data were pedigrees of 25,036 Black-and-White sires born from 1960 through 2000, divided into subsets of 11,447 proven and 13 589 unproven sires, and their 38,228 ancestors, altogether 63,264 animals. Average inbreeding coefficients were about 0.3% for both subsets of sires. Mean relationship coefficients ranged from 0.1% in all animals to 0.7% in the subset of proven sires. Positive time trends in inbreeding coefficients were observed when the subsets of sires were divided into 5-year intervals according to the year of birth and in terms of Holstein Friesian gene contribution.

Animal Husbandry↗