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Anther-stigma separation is associated with inbreeding depression in Datura stramonium, a predominantly self-fertilizing annual.

Genetically based variation in outcrossing rate generates lineages within populations that differ in their history of inbreeding. According to some models, mating-system modifiers in such populations will demonstrate both linkage and identity disequilibrium with fitness loci, resulting in lineage-specific inbreeding depression. Other models assert that differences among families in levels of inbreeding depression are mainly attributable to random accumulation of genetic load, unrelated to variation at mating-system loci. We measured female reproductive success of selfed and outcrossed progeny from naturally occurring lineages of Datura stramonium, a predominantly self-fertilizing annual weed that has heritable variation in stigma-anther separation, a trait that influences selfing rates. Progeny from inbred lineages (as identified by high degree of anther-stigma overlap) showed equal levels of seed production, regardless of cross type. Progeny from mixed lineages (as identified by relatively high separation between anthers and stigma) showed moderate levels of inbreeding depression. We found a significant correlation between anther-stigma separation and relative fitness of selfed and outcrossed progeny, suggesting that family-level inbreeding depression may be related to differences among lineages in inbreeding history in this population. Negative inbreeding depression in putatively inbred lineages may be due in part to additive effects or to epistatic interactions among loci.

Datura stramonium↗

Outcrossing rate and inbreeding depression in the perennial yellow bush lupine, Lupinus arboreus (Fabaceae).

Little is known about the breeding systems of perennial Lupinus species. We provide information about the breeding system of the perennial yellow bush lupine, Lupinus arboreus, specifically determining self-compatibility, outcrossing rate, and level of inbreeding depression. Flowers are self-compatible, but autonomous self-fertilization rarely occurs; thus selfed seed are a product of facilitated selfing. Based on four isozyme loci from 34 maternal progeny arrays of seeds we estimated an outcrossing rate of 0.78. However, when we accounted for differential maturation of selfed seeds, the outcrossing rate at fertilization was lower, ∼0.64. Fitness and inbreeding depression of 11 selfed and outcrossed families were measured at four stages: seed maturation, seedling emergence, seedling survivorship, and growth at 12 wk. Cumulative inbreeding depression across all four life stages averaged 0.59, although variation existed between families for the magnitude of inbreeding depression. Inbreeding depression was not manifest uniformly across all four life stages. Outcrossed flowers produced twice as many seeds as selfed flowers, but the mean performance of selfed and outcrossed progeny was not different for emergence, seedling survivorship, and size at 12 wk. Counter to assumptions about this species, L. arboreus is both self-compatible and outcrosses ∼78% of the time.

Journal Article↗

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↗

Production traits of Holstein cattle: estimation of nonadditive genetic variance components and inbreeding depression.

Additive, dominance, and additive by additive components of genetic variance and inbreeding depression were estimated for production traits from a group of daughters of young sires from the Canadian Holstein population. First lactations of 92,838 cows were analyzed. Three sire and dam models (additive, additive plus dominance, additive plus dominance plus additive by additive genetic effects), all including regression of the trait on inbreeding coefficient of the cow, were used to estimate the effect of inbreeding on production traits. For all production traits, heritability in the narrow sense was overestimated with the simplest model, in which only the additive effect was fitted. Estimates of dominance variance were low for all traits, .9 to 3%. Additive by additive components were low for milk, 2.8%, and fat yield, 2.8%, but higher for protein yield, 6.8%, and for fat, 9%, and protein percentages, 8.9%. Estimates of inbreeding depression for the five traits were similar across all models (-25, -.9, and -.8 kg; .05% and .05% per 1% increase in inbreeding for milk, fat, and protein production and fat and protein percentages, respectively). More accurate estimates of additive effects might be obtained with the inclusion of nonadditive effects for genetic evaluation. If the estimation of inbreeding depression is the only objective, simple models and small random samples of the population may be adequate.

Animals↗

Factors influencing the extent of inbreeding depression: an example from scots pine

Detailed studies suggest that the level of inbreeding depression may vary between populations. In a study of Scots pine from Finland, the level of inbreeding depression was much lower in northern than in southern populations. We have examined theoretically whether population genetic factors, such as the level of selfing, intensity of selection against heterozygotes or homozygotes, level of mutation, a bottleneck, finite population size, or the level of polyembryony could account for this difference. Higher selfing or stronger selection against heterozygotes in the north, both at biologically reasonable levels, appear to produce changes consistent with the observed differences and we consider these to be the most likely explanations. In addition, the differences could have accumulated by these mechanisms over the age of the northern population, approximately 100 generations. Finally, the differences generated by these factors could still be maintained in the face of reasonable levels of gene flow from the south. Such a comprehensive theoretical investigation of this example has given some general insight into the potential influence of these evolutionary factors on the level of inbreeding depression and provides an approach that could be used to understand similar phenomena in other examples.

Journal Article↗

Inbreeding depression in two populations of Arenaria uniflora (Caryophyllaceae) with contrasting mating systems.

I used parallel family-structured crossing designs to investigate the relative performance of self and outcross progeny in selfing and predominantly outcrossing populations of the annual plant Arenaria uniflora. The selfer population experienced much lower inbreeding depression (delta = 0.05 +/- 0.02 SE) than the outcrossers (delta = 0.19 +/- 0.02 SE). The negative association between genetic load and selfing rate suggests that purgable partially recessive alleles are the primary source of inbreeding depression, as does its late expression in both populations. Inbreeding depression in the selfer population, which naturally consists of highly inbred lines, was used to calculate the mean dominance (h = 0.33) and incidence rate (U = 0.30) of deleterious mutations. In the outcrosser population, significant variation among individuals in the expression of inbreeding depression may reflect lineage-specific differences in inbreeding history or, more probably, random variation in mutational load. The low (<< 0.5) inbreeding depression of outcrossers suggests that the maintenance of a mixed mating system in some A. uniflora populations and the evolution of nearly cleistogamous self-pollination in others may reflect local pollinator-mediated selection for selfing rather than the constant 3:2 genetic advantage invoked by many models.

Analysis of Variance↗

Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus).

Evolutionary and conservation biologists have a long-standing interest in the consequences of inbreeding. It is generally recognized that inbred individuals may experience reduced fitness or inbreeding depression. By the same token, relatively outbred individuals can have greater than average fitness, i.e. heterosis. However, nearly all of the empirical evidence for inbreeding depression comes from laboratory or domestic species. Inbreeding depression and heterosis are difficult to detect in natural populations due to the difficulties in establishing pedigrees. An alternative method is to correlate heterozygosity, which is measured using genetic markers, with a trait related to fitness. The typically studied traits, such as juvenile survival and growth rates, either cover only early life or are weakly correlated with lifetime breeding success (LBS). In this paper we show that heterozygosity is positively associated with male and female adult LBS in a wild population of red deer (Cervus elaphus) on the Isle of Rum, Scotland. To the authors' knowledge, this is the first time that inbreeding depression and/or heterosis have been detected for a trait highly correlated with overall fitness in both sexes in a wild population.

Animals↗

Runs of Homozygosity Predict Inbreeding Depression Across Taxa: A Systematic Review and Meta-Analysis.

Measuring inbreeding via runs of homozygosity (ROH) captures realized autozygosity and can infer inbreeding timing through ROH length. A growing body of literature links the proportion of the genome in ROH (FROH) to fitness outcomes across taxa, yet systematic synthesis has been lacking. Here, we conduct a systematic review and meta-analysis to quantify FROH-fitness associations, identify drivers of variation and derive conservation-relevant recommendations. Narrative synthesis of 44 studies revealed that inbreeding depression operates through multiple interconnected pathways (survival, maternal effects, disease susceptibility, reproduction). Critically, purging cannot be relied upon to eliminate inbreeding depression as substantial fitness costs persist even in historically small populations. Meta-analysis of 62 effect sizes revealed a significant negative association between genomic inbreeding and fitness across taxa (Fisher's z&#x2009;=&#x2009;-0.103, r&#x2009;=&#x2009;-0.10, p&#x2009;<&#x2009;0.0001). Study group, whether wildlife, livestock or humans, explained 22.5% of variance, with wildlife showing strongest effects (6-fold stronger than humans). Survival traits showed the greatest sensitivity to the effects of ROH (r&#x2009;=&#x2009;-0.22). Additionally, ROH detection methodology significantly influenced effect sizes: comprehensive approaches (all ROH lengths) detected stronger depression (r&#x2009;=&#x2009;-0.18) than long-ROH-only analyses (r&#x2009;=&#x2009;-0.08, p&#x2009;=&#x2009;0.008), indicating cumulative genetic load matters. Overall, results indicate significant but variable fitness associations with ROH, with effect magnitude depending on biological context and methodological approach. Comprehensive ROH-based approaches show promise as conservation monitoring tools, but limited wildlife studies, particularly for non-mammalian taxa, highlight an urgent need for standardized protocols and expanded empirical research.

Animals↗

Inbreeding depression and heterosis in populations of Schiedea viscosa, a highly selfing species.

Progeny from self-pollinations and intrapopulation crosses were examined in Schiedea viscosa to determine the extent of inbreeding depression in this highly selfing species. Progeny of interpopulation crosses were also investigated to determine whether deleterious alleles have been fixed in populations of S. viscosa. There was no inbreeding depression at early life history stages, including seeds per capsule, seed mass, or germination. Inbreeding depression was detected for the later life history stage of fruit biomass, although not for survival or life span. Heterosis for vegetative biomass and fruit biomass was detected in progeny from crosses between populations. Levels of inbreeding depression in S. viscosa are low relative to out-crossing species of Schiedea, especially when early life history stages are compared.

Age Factors↗

Inbreeding Depression and Genetic Rescue in a Plant Metapopulation.

While migration of individuals has been shown to increase the persistence of small isolated populations through a process known as the "rescue effect," the demographic effects that pollen-mediated gene flow may have in plant populations are not known empirically. This study investigates the role that inbreeding depression plays in newly colonized populations of a common, dioecious, weedy species, Silene alba. Experimental greenhouse studies presented here show that S. alba displays high levels of inbreeding depression (expressed as lowered germination success) in progeny produced with inbreeding coefficients of 0.125 (half-sib mated), 0.250 (full-sib mated), and 0.375 (second-generation sib mated). In addition, it is shown that the degree of inbreeding depression in 12 natural colonies varies with the degree of isolation from other established populations. Significantly, data from experimental populations showed that gene flow into patches comprised of full sibs was higher than those observed into patches comprised of unrelated individuals and may serve to mitigate the effects of inbreeding depression. It is suggested that population connectivity through pollen-mediated gene flow may have substantial effects on the persistence of isolated colonies and on the spatial structure of a metapopulation in general.

gene flow↗

Equivalent inbreeding depression under laboratory and field conditions in a tree-hole-breeding mosquito.

Understanding the consequences of inbreeding has important implications for a wide variety of topics in population biology. However, most studies quantifying the effects of inbreeding are performed under artificial farm, greenhouse, laboratory or zoo conditions. Although several authors have argued that the deleterious effects of inbreeding (inbreeding depression) are likely to be more severe under natural field conditions than in artificial experimental environments, these arguments are usually speculative or based on indirect comparisons. We quantified the effects of inbreeding on fitness traits in a tree-hole-breeding mosquito Aedes geniculatus) under near-optimal laboratory conditions and in three natural tree holes. Our index of fitness (Ro) was lower in the field than in the laboratory and declined due to inbreeding in both However, environments, we found no significant interactions between inbreeding depression and environmental conditions. In both the field and laboratory a 10% increase in the inbreeding coefflicient (F) led to a 12-15) decline in fitness (Ro) These results suggest that inbreeding depression will not necessarily be more extreme under natural field conditions than in the laboratory.

Aedes↗

Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae).

We evaluated the degree of selfing and inbreeding depression at the seed and seedling stages of a threatened tropical canopy tree, Neobalanocarpus heimii, using microsatellite markers. Selection resulted in an overall decrease in the level of surviving selfed progeny from seeds to established seedlings, indicating inbreeding depression during seedling establishment. Mean seed mass of selfed progeny was lower than that of outcrossed progeny. Since the smaller seeds suffered a fitness disadvantage at germination in N. heimii, the reduced seed mass of selfed progeny would be one of the determinants of the observed inbreeding depression during seedling establishment. High selfing rates in some mother trees could be attributed to low local densities of reproductive individuals, thus maintenance of a sufficiently high density of mature N. heimii should facilitate regeneration and conservation of the species.

Ericales↗

Evidence for the partial dominance of viability genes contributing to inbreeding depression in Mimulus guttatus.

The relative importance of different modes of gene expression of viability genes contributing to inbreeding depression was investigated in the wild plant, Mimulus guttatus. Viability genes were identified by self-fertilizing 31 outbred plants, each heterozygous for three to nine unlinked allozyme markers, and analyzing segregation ratios of selfed progeny at maturity for deviations from 1:2:1 ratios. In this study, 24 linkages of viability genes to marker loci were detected. To infer the nature of gene action for these viability genes, a "model-free" graphical method was developed that examines the "space" of segregation ratios allowed by each of seven selection models (i.e., overdominance, complete recessivity, partial recessivity, additivity, partial dominance, complete dominance and underdominance). Using this method, we found that, of 24 linkages detected, 18 were consistent with either partial dominance, complete dominance or underdominance. Six were consistent with either partial recessivity, complete recessivity or overdominance. This finding indicates that, in these chromosomal segments identified by allozyme markers, partial dominance plays the predominant role in inbreeding depression. This is inconsistent with either the dominance or overdominance hypotheses proposed to account for inbreeding depression.

Crosses, Genetic↗

Recent approaches into the genetic basis of inbreeding depression in plants.

Predictions for the evolution of mating systems and genetic load vary, depending on the genetic basis of inbreeding depression (dominance versus overdominance, epistasis and the relative frequencies of genes of large and small effect). A distinction between the dominance and overdominance hypotheses is that deleterious recessive mutations should be purged in inbreeding populations. Comparative studies of populations differing in their level of inbreeding and experimental approaches that allow selection among inbred lines support this prediction. More direct biometric approaches provide strong support for the importance of partly recessive deleterious alleles. Investigators using molecular markers to study quantitative trait loci (QTL) often find support for overdominance, though pseudo-overdominance (deleterious alleles linked in repulsion) may bias this perception. QTL and biometric studies of inbred lines often find evidence for epistasis, which may also contribute to the perception of overdominance, though this may be because of the divergent lines initially crossed in QTL studies. Studies of marker segregation distortion commonly uncover genes of major effect on viability, but these have only minor contributions to inbreeding depression. Although considerable progress has been made in understanding the genetic basis of inbreeding depression, we feel that all three aspects merit more study in natural plant populations.

Epistasis, Genetic↗

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 depression due to mildly deleterious mutations in finite populations: size does matter.

We studied the effects of population size on the inbreeding depression and genetic load caused by deleterious mutations at a single locus. Analysis shows how the inbreeding depression decreases as population size becomes smaller and/or the rate of inbreeding increases. This pattern contrasts with that for the load, which increases as population size becomes smaller but decreases as inbreeding rate goes up. The depression and load both approach asymptotic limits when the population size becomes very large or very small. Numerical results show that the transition between the small and the large population regimes is quite rapid, and occurs largely over a range of population sizes that vary by a factor of 10. The effects of drift on inbreeding depression may bias some estimates of the genomic rate of deleterious mutation. These effects could also be important in the evolution of breeding systems in hermaphroditic organisms and in the conservation of endangered populations.

Genetics, Population↗

Inbreeding depression influences genet size distribution in a marine angiosperm.

Although inbreeding depression is a major genetic phenomena influencing individual fitness, it is difficult to measure in wild populations. An alternative approach is to correlate heterozygosity, measured using highly polymorphic markers, with a fitness-correlated trait. In clonal plants, genet size is predicted to be fitness correlated. Here we test the prediction that the genet size distribution of the marine clonal plant Zostera marina (eelgrass) is influenced by inbreeding depression. We used nine polymorphic microsatellite markers to access the fine scale clonal structure and to measure individual heterozygosity within 4 plots (each corresponds to 256 m2, sampled at 1-m intervals) in two populations along the German Baltic Coast. The same plots were also sampled for flowering and vegetative shoots to obtain estimates for sexual reproductive output at the level of the genetic individual. We found substantial differences in the genet size distribution between the two populations that may be explained by different disturbance frequency. In both populations, clone size was significantly positively correlated with the total number of flowering shoots, indicating that larger clones have a higher reproductive output. Individual heterozygosity was significantly positively associated with clone size. The effect was much stronger in Falkenstein (low disturbance) than in Maasholm (high disturbance). The results indicate that in a low disturbance population the relatively outbred clones occupy a higher proportion of the available space, possibly because they outcompete relatively inbred neighbours.

Alleles↗

Evidence for inbreeding depression in the food-deceptive colour-dimorphic orchid Dactylorhiza sambucina (L.) Soò.

About one third of all orchid species are deceptive, i.e., not providing any reward to their pollinator. Such species often have lower visitation rates compared to rewarding relatives. This could result in lower levels of geitonogamous selfing and thus would provide an advantage in term of progeny fitness through inbreeding avoidance. This hypothesis could be tested by comparing the level of inbreeding depression between deceptive and rewarding orchids. However, due to the difficulty to raise orchids from seeds, few studies of inbreeding depression are available, and most are focused on very early life stages, such as seed mass or embryo viability. Here, we present the results from an experimental investigation of inbreeding depression in the deceptive flower-colour dimorphic Dactylorhiza sambucina, from in vitro cultivation to greenhouse soil transplantation. We found strong inbreeding depression at all recorded stages (i.e., germination and survival), with estimates ranging from 0.47 to 0.75. Our study finally proposes a simple and suitable experimental protocol to raise orchids from seeds with high germination rates.

Color↗