Inbreeding depression and outbreeding depression in Digitalis purpurea: optimal outcrossing distance in a tetraploid

An optimal crossing distance exists within plant populations if inbreeding and outbreeding depression operate simultaneously. In a population of tetraploid Digitalis purpurea, maternal plants were pollinated with donors at four distances: 0 (self-pollination), 1, 6 and 30 m. Lifetime fitness of F1 progeny was investigated in greenhouse experiments, and significant inbreeding and outbreeding depression were detected at five vs. three life history traits. Inbreeding depression increased at later life stages, whereas outbreeding depression was relatively constant. The existence of within-population outbreeding depression suggests substantial genetic structuring at moderate distances in D. purpurea, and corroborates recent findings of significant outbreeding depression in F1 progeny in polyploids. The moderate inbreeding depression found in this predominately outcrossing population supports the notion that effects of inbreeding are less severe in polyploids than in diploids.     

Inbreeding depression in Lychnis flos-cuculi (Caryophyllaceae): effects of different levels of inbreeding

In a controlled crossing experiment on Lychnis flos-cuculi plants in the greenhouse, outbred and selfed maternal plants were each treated with pollen from unrelated plants, siblings and selves. The seeds thus obtained had expected inbreeding coefficients of 0, 0.25 and 0.5 for the outbred maternal plants, and 0, 0.5 and 0.75 for the selfed maternal plants. Seed abortion rate, seed weight and germination rate were estimated. Seedlings were transplanted to an outdoor garden, and monitored for survival, probability of flowering, number of capsules and area of capsules next spring. Inbred seeds germinated slower and in lower proportions than those less inbred, and seedlings had lower survival, flowering, fruit set and area of capsules if inbred. Combined fitness values were estimated from the survival and fecundity components, and severe inbreeding depression was detected for these estimates (0.51 and 0.56 for one generation of selfing). The fitness function decreased linearly with the increase in inbreeding coefficient, which is as expected if the inbreeding depression is additive among loci.     

Inbreeding depression in an asexual population of Mimulus guttatus

The reproductive mechanism, that is whether an organism outcrosses, selfs or asexually reproduces, has a substantial impact on the amount and pattern of genetic variation. In this study, we estimate genetic variation and genetic load for a predominately asexual population of Mimulus guttatus, and then compare our results to other studies of predominately sexually reproducing (outcrossing and selfing) populations of M. guttatus. The asexual population had low levels of heterozygosity (H_e = 0.03) and low (but significantly non‐zero) inbreeding load, especially when compared with other M. guttatus populations. This differs greatly from the sexual populations of Mimulus that display substantial inbreeding depression. We discuss a variety of reasons why we see such low load in this study and suggest future research projects to further explore the questions.     

Inbreeding depression along a life-history continuum in the great tit

Inbreeding resulting from the mating of two related individuals can reduce the fitness of their progeny. However, quantifying inbreeding depression in wild populations is challenging, requiring large sample sizes, detailed knowledge of life histories and study over many generations. Here we report analyses of the effects of close inbreeding, based on observations of mating between relatives, in a large, free-living noninsular great tit (Parus major) population monitored over 41 years. Although mating between close relatives (f > or = 0.125) was rare (1.0-2.6% of matings, depending on data set restrictiveness), we found pronounced inbreeding depression, which translated into reduced hatching success, fledging success, recruitment to the breeding population and production of grand offspring. An inbred mating at f = 0.25 had a 39% reduction in fitness relative to that of an outbred nest, when calculated in terms of recruitment success, and a 55% reduction in the number of fledged grand offspring. Our data show that inbreeding depression acts independently at each life-history stage in this population, and hence suggest that estimates of the fitness costs of inbreeding must focus on the entire life cycle.     

Inbreeding depression and mixed mating in Leptosiphon jepsonii: a comparison of three populations

BACKGROUND AND AIMS: Inbreeding depression is thought to play a central role in the evolution and maintenance of cross-fertilization. Theory indicates that inbreeding depression can be purged with self-fertilization, resulting in positive feedback for the selection of selfing. Variation among populations of Leptosiphon jepsonii in the timing and rate of self-fertilization provides an opportunity to study the evolution of inbreeding depression and mating systems. In addition, the hypothesis that differences in inbreeding depression for male and female fitness can stabilize mixed mating in L. jepsonii is tested. METHODS: In a growth room experiment, inbreeding depression was measured in three populations with mean outcrossing rates ranging from 0.06 to 0.69. The performance of selfed and outcrossed progeny is compared at five life history stages. To distinguish between self-incompatibility and early inbreeding depression, aborted seeds and unfertilized ovules were counted in selfed and outcrossed fruits. In one population, pollen and ovule production was quantified to estimate inbreeding depression for male and female fitness. KEY RESULTS: Both prezygotic barriers and inbreeding depression limited self seed set in the most outcrossing population. Cumulative inbreeding depression ranged from 0.297 to 0.501, with the lowest value found in the most selfing population. Significant inbreeding depression for early life stages was found only in the more outcrossing populations. Inbreeding depression was not significant for pollen or ovule production. CONCLUSIONS: The results provide modest support for the hypothesized relationship between inbreeding depression and mating systems. The absence of early inbreeding depression in the more selfing populations is consistent with theory on purging. Differences in male and female expression of inbreeding depression do not appear to stabilize mixed mating in L. jepsonii. The current estimates of inbreeding depression for L. jepsonii differ from those of previous studies, underscoring the effects of environmental variation on its expression.     

Inbreeding,inbreeding depression,and infidelity in a cooperatively breeding bird*

Inbreeding depression plays a major role in shaping mating systems: in particular, inbreeding avoidance is often proposed as a mechanism explaining extra‐pair reproduction in socially monogamous species. This suggestion relies on assumptions that are rarely comprehensively tested: that inbreeding depression is present, that higher kinship between social partners increases infidelity, and that infidelity reduces the frequency of inbreeding. Here, we test these assumptions using 26 years of data for a cooperatively breeding, socially monogamous bird with high female infidelity, the superb fairy‐wren (Malurus cyaneus). Although inbred individuals were rare (～6% of offspring), we found evidence of inbreeding depression in nestling mass (but not in fledgling survival). Mother–son social pairings resulted in 100% infidelity, but kinship between a social pair did not otherwise predict female infidelity. Nevertheless, extra‐pair offspring were less likely to be inbred than within‐pair offspring. Finally, the social environment (the number of helpers in a group) did not affect offspring inbreeding coefficients or inbreeding depression levels. In conclusion, despite some agreement with the assumptions that are necessary for inbreeding avoidance to drive infidelity, the apparent scarcity of inbreeding events and the observed levels of inbreeding depression seem insufficient to explain the ubiquitous infidelity in this system, beyond the mother–son mating avoidance.     

Inbreeding and inbreeding depression of early life traits in a cooperative mammal

Mating between relatives often results in negative fitness consequences or inbreeding depression. However, the expression of inbreeding in populations of wild cooperative mammals and the effects of environmental, maternal and social factors on inbreeding depression in these systems are currently not well understood. This study uses pedigree‐based inbreeding coefficients from a long‐term study of meerkats (Suricata suricatta) in South Africa to reveal that 44% of the population have detectably non‐zero (F > 0) inbreeding coefficients. 15% of these inbred individuals were the result of moderate inbreeding (F ≥ 0.125), although such inbreeding events almost solely occurred when mating individuals had no prior experience of each other. Inbreeding depression was evident for a range of traits: pup mass at emergence from the natal burrow, hind‐foot length, growth until independence and juvenile survival. However, we found no evidence of significant inbreeding depression for skull and forearm length or for pup survival. This research provides a rare investigation into inbreeding in a cooperative mammal, revealing high levels of inbreeding, considerable negative consequences and complex interactions with the social environment.     

Inbreeding in the Seychelles warbler: environment-dependent maternal effects

The deleterious effects of inbreeding can be substantial in wild populations and mechanisms to avoid such matings have evolved in many organisms. In situations where social mate choice is restricted, extrapair paternity may be a strategy used by females to avoid inbreeding and increase offspring heterozygosity. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, neither social nor extrapair mate choice was used to avoid inbreeding facultatively, and close inbreeding occurred in approximately 5% of matings. However, a higher frequency of extra-group paternity may be selected for in female subordinates because this did reduce the frequency of mating between close relatives. Inbreeding resulted in reduced individual heterozygosity, which, against expectation, had an almost significant (P = 0.052), positive effect on survival. Conversely, low heterozygosity in the genetic mother was linked to reduced offspring survival, and the magnitude of this intergenerational inbreeding depression effect was environment-dependent. Because we controlled for genetic effects and most environmental effects (through the experimental cross-fostering of nestlings), we conclude that the reduced survival was a result of maternal effects. Our results show that inbreeding can have complicated effects even within a genetic bottlenecked population where the "purging" of recessive alleles is expected to reduce the effects of inbreeding depression.     

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.     

Genomic analysis reveals depression due to both individual and maternal inbreeding in a free‐living mammal population

There is ample evidence for inbreeding depression manifested as a reduction in fitness or fitness‐related traits in the focal individual. In many organisms, fitness is not only affected by genes carried by the individual, but also by genes carried by their parents, for example if receiving parental care. While maternal effects have been described in many systems, the extent to which inbreeding affects fitness directly through the focal individual, or indirectly through the inbreeding coefficients of its parents, has rarely been examined jointly. The Soay sheep study population is an excellent system in which to test for both effects, as lambs receive extended maternal care. Here, we tested for both maternal and individual inbreeding depression in three fitness‐related traits (birthweight and weight and hindleg length at 4 months of age) and three fitness components (first‐year survival, adult annual survival and annual breeding success), using either pedigree‐derived inbreeding or genomic estimators calculated using ~37 000 SNP markers. We found evidence for inbreeding depression in 4‐month hindleg and weight, first‐year survival in males, and annual survival and breeding success in adults. Maternal inbreeding was found to depress both birthweight and 4‐month weight. We detected more instances of significant inbreeding depression using genomic estimators than the pedigree, which is partly explained through the increased sample sizes available. In conclusion, our results highlight that cross‐generational inbreeding effects warrant further exploration in species with parental care and that modern genomic tools can be used successfully instead of, or alongside, pedigrees in natural populations.     

Inbreeding depression and low between-population heterosis in recently diverged experimental populations of a selfing species

In fragmented populations, genetic drift and selection reduce genetic diversity, which in turn results in a loss of fitness or in a loss of evolvability. Genetic rescue, that is, controlled input of diversity from distant populations, may restore evolutionary potential, whereas outbreeding depression might counteract the positive effect of this strategy. We carried out self-pollination and crosses within and between populations in an experimental subdivided population of a selfing species, Triticum aestivum L., to estimate the magnitude of these two phenomena. Surprisingly, for a self-fertilizing species, we found significant inbreeding depression within each population for four of the six traits studied, indicating that mildly deleterious mutations were still segregating in these populations. The progeny of within- and between-population crosses was very similar, indicating low between-population heterosis and little outbreeding depression. We conclude that relatively large population effective sizes prevented fixation of a high genetic load and that local adaptation was limited in these recently diverged populations. The kinship coefficient estimated between the parents using 20 neutral markers was a poor predictor of the progeny phenotypic values, indicating that there was a weak link between neutral diversity and genes controlling fitness-related traits. These results show that when assessing the viability of natural populations and the need for genetic rescue, the use of neutral markers should be complemented with information about the presence of local adaptation in the subdivided population.     

Inbreeding depression effects on extinction time in a predator—prey system

Summary Traditional methods of assessing population viability ignore both genetic—demographic interactions as well as community level dynamics. We address these deficiencies by presenting a model that investigates the effects of predation on a prey population experiencing inbreeding depression. Beginning with a simple Lotka—Volterra predator—prey system, we rewrite prey per capita mortality as a function of inbreeding. Inbreeding varies as a function of population size. Using computer simulation, we find that prey extinction times are inversely related to the level of inbreeding depression with and without predation. For all but very low levels of inbreeding depression, predation appreciably reduces persistence time. At moderate levels of inbreeding, predators go extinct before prey. When migration is introduced at low and moderate rates, persistence times only improve for those populations with low inbreeding depression measures. At a higher migration rate, persistence times are lengthened for low and moderately depressed prey populations. Increasing birth rates produce a visible, though noisy, trend towards increased times to extinction for low to moderate levels of inbreeding.     

Pollen limitation and inbreeding depression in an 'old rare' bumblebee-pollinated grassland herb

Habitat fragmentation and reduction of population size have been found to negatively affect plant reproduction in 'new rare' species that were formerly common. This has been attributed primarily to effects of increased inbreeding but also to pollen limitation. In contrast, little is known about the reproduction of 'old rare' species that are naturally restricted to small and isolated habitats and thus may have developed strategies to cope with long-term isolation and small population size. Here we study the effects of pollen source and quantity on reproduction of the 'old rare' bumblebee-pollinated herb, Astragalus exscapus. In two populations of this species, we tested for pollen autodeposition, inbreeding depression and outbreeding depression. Caged plants were left unpollinated or were pollinated with pollen from the same plant, from the same population or from a distant population (50 km). Additionally, we tested for pollen limitation by pollen supplementation in four populations of different size and density. In the absence of pollinators, plants did not produce seed whereas self-pollinated plants did. This indicates a self-compatible breeding system dependent on insect pollination. Both self-pollination and, in one of the two populations, cross-pollination with pollen from plants from the distant population resulted in a lower number of seeds per flower than cross-pollination with pollen from plants from the resident population, indicating inbreeding and outbreeding depression. Pollen addition enhanced fruit set and number of seeds per flower in three of the four populations, indicating pollen limitation. The degree of pollen limitation was lowest in the smallest but densest population. Our results suggest that, similar to 'new rare' plant species, also 'old rare' species may be at risk of inbreeding depression and pollen limitation.     

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.     

Long-term progression of inbreeding depression in a Mediterranean ornithophilous shrub

The ornithophilous species Anagyris foetida L. is a Mediterranean shrub with highly fragmented populations and a mixed mating system. In a previous study, we analyzed the first 3 years of the life cycle of two progenies (selfed and outcrossed) grown from seed obtained by hand pollination and planted in an experimental garden in 2005. In that study, we found that inbreeding depression (ID) was manifested both reproductively and vegetatively throughout the life cycle, with male reproductive function being the most affected trait. In the present study, our main aim was to check the progression of the two progenies 12 years after transplantation. For this we analyzed their survival and their vegetative and reproductive traits. According to our results, levels of ID were similar to those obtained in the previous study, with some factors decreased and thus varying with the age of the studied individuals. Vegetative parameters were found to have a greater influence than reproductive ones (δ = 0.56 vs. δ = 0.36) on overall ID. As indicated by the global ID (δ = 0.72) the populations have a mating system that is intermediate between outcrossing and a mixed system. Furthermore, the lower male reproductive capacity of the selfed individuals has been maintained over time. Our study also demonstrates the importance of studying the ID value throughout the life cycle of plants.     

Inbreeding depression in self-incompatible North-American Arabidopsis lyrata: disentangling genomic and S-locus-specific genetic load

Newly formed selfing lineages may express recessive genetic load and suffer inbreeding depression. This can have a genome-wide genetic basis, or be due to loci linked to genes under balancing selection. Understanding the genetic architecture of inbreeding depression is important in the context of the maintenance of self-incompatibility and understanding the evolutionary dynamics of S-alleles. We addressed this using North-American subspecies of Arabidopsis lyrata. This species is normally self-incompatible and outcrossing, but some populations have undergone a transition to selfing. The goals of this study were to: (1) quantify the strength of inbreeding depression in North-American populations of A. lyrata; and (2) disentangle the relative contribution of S-linked genetic load compared with overall inbreeding depression. We enforced selfing in self-incompatible plants with known S-locus genotype by treatment with CO₂, and compared the performance of selfed vs outcrossed progeny. We found significant inbreeding depression for germination rate (δ=0.33), survival rate to 4 weeks (δ=0.45) and early growth (δ=0.07), but not for flowering rate. For two out of four S-alleles in our design, we detected significant S-linked load reflected by an under-representation of S-locus homozygotes in selfed progeny. The presence or absence of S-linked load could not be explained by the dominance level of S-alleles. Instead, the random nature of the mutation process may explain differences in the recessive deleterious load among lineages.     

Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster

Recent meta-analyses conducted across a broad range of taxa have demonstrated a strong linear relationship between the change in magnitude of inbreeding depression under stress and stress level, measured as fitness loss in outbred individuals. This suggests that a general underlying response may link stress and inbreeding depression. However, this relationship is based primarily on laboratory data, and it is unknown whether natural environments with multiple stressors and fluctuating stress levels alter how stress affects inbreeding depression. To test whether the same pattern persists in the field, we investigated the effect of seasonal variation on stress level and inbreeding depression in a 3-year field study measuring the productivity of captive populations of inbred and outbred Drosophila melanogaster. We found cold winter temperatures were most stressful and induced the greatest inbreeding depression. Furthermore, these data, collected under natural field conditions, conformed to the same predictive linear relationship seen in Drosophila laboratory studies, with inbreeding depression increasing by 0.17 lethal equivalents for every 10 per cent increase in stress level. Our results suggest that under natural conditions stress level is a primary determinant of the magnitude of inbreeding depression and should be considered when assessing extinction vulnerability in small populations.     

Reduced inbreeding depression in peripheral relative to central populations of a monocarpic herb

Many temperate taxa were confined to warmer latitudes during the last glacial maximum. As their ranges expanded when climates warmed, genetic drift and inbreeding in relatively small peripheral populations are expected to have reduced genetic diversity and the segregating genetic load. Therefore, inbreeding depression in peripheral populations might be lower than in centrally located sites. We evaluated the consequences of inbreeding for fitness traits in six central and six northern peripheral populations of the herb Campanulastrum americanum. Inbreeding reduced performance for all traits. Inbreeding depression in peripheral populations was lower than in central populations. This difference increased across the life cycle from similar levels for germination, to central populations having three times the inbreeding depression for adult traits. Geographical patterns of inbreeding depression suggest that mating system variation and potential future mating system evolution in many temperate taxa might reflect, at least in part, nonequilibrium conditions associated with historic range changes.     

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.     

Inbreeding and inbreeding depression in a threatened endemic plant,the African violet (Saintpaulia ionantha ssp. grotei), of the East Usambara Mountains,Tanzania

Mating among closely‐related individuals in small and isolated plant populations may result in reduced vigour of the inbred offspring, i.e. inbreeding depression, especially in naturally outbreeding plants. Occurrence of inbreeding and inbreeding depression was studied in Saintpaulia ionantha ssp. grotei, a threatened endemic plant species with a narrow ecological amplitude from the East Usambara Mountains. The level of inbreeding (measured as the fixation index, F) was investigated in twelve populations by analyzing variation at one microsatellite marker locus. The effect of one generation of selfing and outcrossing on the progeny fitness was studied by controlled crosses in two small patches that differ in the level isolation. The fixation index (F) across the populations was on the average 0.21 and varied among the populations from substantial inbreeding (F = 0.58) to surplus heterozygosity (F = −0.29). High inbreeding depression (δ) was observed at early and late stages of the life‐cycle. The isolated patch exhibited lower inbreeding depression than did the non‐isolated patch. The results of this study suggest that inbreeding and subsequent inbreeding depression are potential threats to the survival of Saintpaulia populations.