Inbreeding depression and mating-distance dependent offspring fitness in large and small populations of Lychnis flos-cuculi (Caryophyllaceae)

The spatial structure of four Lychnis flos-cuculi populations, varying in size and degree of isolation, was studied by comparing the fitness of offspring resulting from self-pollination and pollinations by neighbouring plants, plants within the same population, and plants from other populations. Selfed offspring had the lowest fitness of the four offspring groups. No significant difference was found between the performance of offspring from pollinations by neighbouring plants and offspring pollinated by plants further apart but within the same population. A lower fitness of offspring from pollinations between neighbours would be expected if these matings, on average, yielded inbred offspring which suffered from inbreeding depression. These results imply that either a tight neighbourhood structuring is not present, or that the inbreeding depression for offspring by neighbours is too low to detect, although these are inbred. Crossings between populations produced offspring with a significantly higher fitness than offspring sired within populations. There were no significant differences in response to inbreeding among the populations, and differences in mean fitness among populations had no clear relation to the population size or degree of isolation. A reduced fitness of small populations due to inbreeding depression or a less severe response to experimental inbreeding due to purging of deleterious alleles is therefore not supported by our results.     

Parental effects in Lychnis flos-cuculi. I: Seed size,germination and seedling performance in a controlled environment

Selection responses in natural plant populations depend on how the phenotypic variation of traits is composed. The contributions of nuclear genetic, maternal, paternal, environmental and inbreeding effects to variation in time to germination, germination percentage, and seed- and seedling size were studied in a population of Lychnis flos-cuculi. It was found that: (1) Maternal effects predominated in the determination of progeny seed size and germination characteristics; (2) Maternal environment during seed development was less important than maternal genotype; (3) Small but significant variation within maternal families could be observed among individuals sired by different fathers; (4) Additive genetic variance was significant for seedling size 4 weeks after germination. In conclusion, selection shortly after emergence will mainly favour particular maternal genotypes, while selection later in the life cycle may act upon zygotic genotypes. Inbreeding depression was significant, especially for vegetative growth. Consistent differences were found among maternal genotypes in the degree of variation in the time to germination, suggesting that selection could operate to favour polymorphic or uniform germination behaviour.     

Parental effects in Lychnis flos-cuculi. II: Selection on time of emergence and seedling performance in the field

Selection on the timing of seedling emergence was investigated in an experimental population of Lychnis flos-cuculi, a perennial hay-meadow species. Seeds obtained from a full diallel cross of 8 genotypes from a field population were sown along an environment gradient that included the parental site. Significant directional selection for early emergence was found and the intensity of selection varied among sites. Emergence time varied significantly among progeny families of different maternal and paternal genotypes. These differences could be attributed to parental effects whereas narrow-sense heritabilities were close to zero. Survivorship until autumn differed among progeny of paternal families. Survivorship of maternal progeny varied among sites. Whereas differences in survival and plant size among individuals from different emergence cohorts persisted over the winter, the significance of these differences among progeny from different parental genotypes disappeared. It is suggested that a response to selection on emergence time might be low since (1) the narrow sense heritability was low, (2) parental genotypes differed in their effect on offspring emergence time when used as female parent or as pollen donor and (3) there was a family x site interaction for survival. Families with relatively early emerging seedlings also had a significantly higher seed weight, emergence percentage, and plant weight although the strength of these among-family correlations varied among sites. It is therefore not likely that simultaneous selection on emergence time and either of these traits would retard a response to selection on emergence time.     

DROUGHT STRESS AND INBREEDING DEPRESSION IN LYCHNIS FLOS-CUCULI (CARYOPHYLLACEAE)

Interactions between drought stress and inbreeding depression were studied in Lychnis flos-cuculi. Four inbreeding levels (F = 0, 0.25, 0.50 and 0.75), and three watering treatments were used. Performance was scored for germination rate and proportion, survival, plant size, proportion of plants flowering, flowering date, stem height, number of flowers, flower size, anther weight, fruiting proportion and number of capsules. Multiplicative fitness values were estimated from these traits. Inbreeding affected most of the traits studied, and a severe inbreeding depression was found for the combined fitness estimates. The higher inbreeding depression found here relative to the same family groups in a former experiment may reflect greater dominance and suppression in the present experiment at higher density.     

Developmental instability in hybrids between Lychnis viscaria and Lychnis alpina (Caryophyllaceae)

Developmental instability shown by increased fluctuating asymmetry can be caused by either genetic or environmental stress. Genomic coadaptation and heterozygosity are the genetic factors that are commonly assumed to increase the level of developmental stability. Therefore, in hybrid populations the level of fluctuating asymmetry (FA) can be lower due to higher heterozygosity or higher due to disruption of coadapted gene complexes, depending on the degree of divergence between hybridizing taxa. Here I present data on FA in petals from hybrids between Lychnis viscaria (Caryophyllaceae) and Lychnis alpina and from parental species grown in a common garden environment. Petal asymmetry of hybrids was clearly higher than that of either parental species grown in common environment. Between the two parental species petal asymmetry did not differ. The mean size of the petals in hybrids was about the same as in L. viscaria, thus indicating no heterotic effect. Therefore, it seems that hybrids between L. viscaria and L. alpina do suffer from the disruption of coadapted gene complexes as indicated by higher developmental instability.     

Inbreeding and inbreeding depression in endangered red wolves (Canis rufus)

In natural populations, the expression and severity of inbreeding depression can vary widely across taxa. Describing processes that influence the extent of inbreeding and inbreeding depression aid in our understanding of the evolutionary history of mating systems such as cooperative breeding and nonrandom mate selection. Such findings also help shape wildlife conservation theory because inbreeding depression reduces the viability of small populations. We evaluated the extent of inbreeding and inbreeding depression in a small, re‐introduced population of red wolves (Canis rufus) in North Carolina. Since red wolves were first re‐introduced in 1987, pedigree inbreeding coefficients (f) increased considerably and almost every wild born wolf was inbred (average f = 0.154 and max f = 0.383). The large inbreeding coefficients were due to both background relatedness associated with few founders and numerous close relative matings. Inbreeding depression was most evident for adult body size and generally absent for direct fitness measures such as reproductive success and survival; no lethal equivalents (LE = 0.00) were detected in juvenile survival. The lack of strong inbreeding depression in direct measures of fitness could be due to a founder effect or because there were no outbred individuals for comparison. Our results highlight the variable expression of inbreeding depression across traits and the need to measure a number of different traits when evaluating inbreeding depression in a wild population.     

Inbreeding and outbreeding effects on pollen fitness and zygote survival in Silene nutans (Caryophyllaceae)

In plants, selfing and outcrossing may be affected by maternal mate choice and competition among pollen and zygotes. To evaluate this in Silene nutans, we pollinated plants with mixtures of (1) self‐ and outcross pollen and (2) pollen from within a population and from another population. Pollen fitness and zygote survival was estimated from the zygote survival and paternity of seeds. Self pollen had a lower fitness than outcross pollen, and selfed zygotes were less likely, or as likely, to develop into seeds. Hybrid zygotes survived as frequently or more than local zygotes, and pollen from one of the populations fertilized most ovules in both populations. Our results thus indicate strong maternal discrimination against selfing, whereas the success of outbreeding seems mostly affected by divergent pollen performance. The implications for the evolution of maternal mate choice are discussed.     

Inbreeding depression in perennial Lychnis viscaria (Caryophyllaceae): effects of population mating history and nutrient availability

We studied inbreeding depression in a perennial plant, Lychnis viscaria, in three populations differing in their inbreeding history and population size by measuring several traits at two nutrient levels over the plant's life cycle. The observed levels of inbreeding depression (cumulative inbreeding depression, from -0.057 to 0.629) were high for a plant with a mixed mating system. As expected, the population with a low level of isozyme variation expressed the least inbreeding depression for seed germination. Highest inbreeding depression for germination was found in the largest and genetically most variable population. No clear differences between populations in expression of inbreeding depression in the later life stages were found. The population level inbreeding depression varied with the nutrient conditions and among populations and life stages, but we found no evidence that inbreeding depression increased with lower nutrient availability. These results emphasize the importance of measuring inbreeding depression under several environmental conditions and over life stages.     

Inbreeding and extinction: Effects of rate of inbreeding

Deleterious alleles may be removed (purged) bynatural selection in populations undergoinginbreeding. However, there is controversyregarding the effectiveness of selection inreducing the risk of extinction due toinbreeding, especially in relation to the rateof inbreeding. We evaluated the effect of therate of inbreeding on reducing extinction risk,in populations of Drosophila melanogastermaintained using full-sib mating (160replicates), or at effective population sizes(N _e) of 10 (80) or 20 (80).Extinction rates in the populations maintainedusing full-sib mating occurred at lower levelsof inbreeding than in the larger populations,whereas the two larger populations did notdiffer significantly from each other.Inbreeding coefficients at 50% extinction were0.62, 0.79 and 0.77 for the full-sib (N _e = 2.6), N _e = 10 and N _e = 20 treatments, respectively. Populations of N _e = 20 that remained extant after 60 generations, showed inbreeding depression, with the mean fitness of these populations being only 45% of the outbredcontrols. There was considerable variationamong the 31 inbred populations in fitness, butnone of the N _e = 20 populations hadfitness that was higher than the outbredcontrol. We conclude that purging may slow therate of extinction slightly, but it cannot berelied on to eliminate the deleterious effectsof inbreeding.     

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,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 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.     

Characterization of microsatellite loci in Lychnis flos‐cuculi (Caryophyllaceae)

We cloned microsatellite repeats from ragged robin Lychnis flos‐cuculi (Caryophyllaceae) and developed 20 primer pairs for microsatellite marker analysis. We used 18 individuals of a large Swiss population to screen microsatellites. Seven loci were polymorphic. Between seven and 11 alleles were found per locus and the observed heterozygosity was between 0.308 and 0.813. Observed heterozygote deficits were significant in five of the seven loci, in line with the mixed mating system of L. flos‐cuculi.     

Inbreeding depression and selfing rates in a self-compatible,hermaphroditic species,Schiedea membranacea (Caryophyllaceae)

Inbreeding depression and selfing rates were investigated in Schiedea membranacea (Caryophyllaceae), a hermaphroditic species endemic to the Hawaiian Islands. Most theoretical models predict high inbreeding depression in outcrossing hermaphroditic species and low inbreeding depression in inbreeding species. Although high outcrossing rates and high levels of inbreeding depression are characteristic of many species of Schiedea, self- fertilization is common among relatives of hermaphroditic S. membranacea, and high selfing rates and low levels of inbreeding depression were predicted in this species. Sixteen individuals grown in the greenhouse were used to produce selfed and outcrossed progeny. Inbreeding depression, which was evident throughout the stages measured (percentage viable seeds per capsule, mean seed mass, percentage seed germination, percentage seedling survival, and biomass after 8 mo), averaged 0.70. Inbreeding depression among maternal families varied significantly for all measured traits and ranged from −0.12 to 0.97. Using isozyme analysis, the multilocus selfing rate varied from 0.13 to 0.38 over 4 yr. Contrary to the initial prediction of high selfing and low inbreeding depression based on phylogenetic relationships within Schiedea, low selfing rates and high levels of inbreeding depression were found in S. membranacea. These results indicate that outcrossing is stable in this species and maintained by high levels of inbreeding depression.     

Variation in the intensity of inbreeding depression among successive life-cycle stages and generations in gynodioecious Silene vulgaris (Caryophyllaceae)

Inbreeding depression is one of the hypotheses explaining the maintenance of females within gynodioecious plant populations. However, the measurement of fitness components in selfed and outcrossed progeny depends on life-cycle stage and the history of inbreeding. Comparative data indicate that strong inbreeding depression is more likely to occur at later life-cycle stages. We used hermaphrodite individuals of Silene vulgaris originating from three populations located in different valleys in the Swiss Alps to investigate the effect of two generations of self- and cross-fertilization on fitness components among successive stages of the life cycle in a glasshouse experiment. We detected significant inbreeding depression for most life-cycle stages including: the number of viable and aborted seeds per fruit, probability of germination, above ground biomass, probability of flowering, number of flowers per plant, flower size and pollen viability. Overall, the intensity of inbreeding depression increased among successive stages of the life cycle and cumulative inbreeding depression was significantly stronger in the first generation (delta approximately 0.5) compared with the second generation (delta approximately 0.35). We found no evidence for synergistic epistasis in our experiment. Our finding of more intense inbreeding depression during later stages of the life cycle may help to explain the maintenance of females in gynodioecious populations of S. vulgaris because purging of genetic load is less likely to occur.     

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.     

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 on beef cattle traits: Estimates,linearity of effects and heterogeneity among sire-families

Records from up to 19054 registered cows and 10297 calves in 155 herds of the Alentejana cattle breed were used to study the effects of individual (F_i) and maternal (F_m) inbreeding on reproductive, growth and carcass traits, as well as assessing the importance of non-linear associations between inbreeding and performance, and evaluating the differences among sire-families in the effect of F_i and F_m on calf weight at 7 months of age (W7M). Overall, regression coefficients of performance traits on inbreeding were small, indicating a minor but still detrimental effect of both F_i and F_m on most traits. The traits with the highest percentage impact of F_i were total number of calvings through life and calf weight at 3 months of age (W3M), followed by longevity and number of calves produced up to 7 years, while the highest effect of F_m was on W3M. Inbreeding depression on feed efficiency and carcass traits was extremely small and not significant. No evidence was found of a non-linear association between inbreeding and performance for the traits analyzed. Large differences were detected among sire-families in inbreeding depression on W7M, for both F_i and F_m, encouraging the possibility of incorporating sire effects on inbreeding depression into selection decisions.