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Selection-mutation balance in polysomic tetraploids: impact of double reduction and gametophytic selection on the frequency and subchromosomal localization of deleterious mutations.

We modeled the behavior of recessive mutations with deleterious effects to either the sporophyte or the gametophyte, or both, in polysomic tetraploid populations by allowing for varying levels of double reduction, mutation, and self-fertilization. Double reduction causes a decrease of the equilibrium frequencies of deleterious alleles, and it has much more influence on genes subjected to gametophytic selection than on genes solely under sporophytic selection. With gametophytic selection, low frequencies of double reduction are enough to reduce equilibrium frequencies severalfold. Double reduction occurs when sister alleles migrate to the same gamete during meiosis. It depends on the frequency at which a locus recombines with its centromere, and on the frequency of multivalent formation. Therefore, a greater accumulation of deleterious mutations should occur on polysomic chromosomes with a prevalence of bivalent pairing and in chromosomal regions between centromeres and proximal chiasmata. Proximal loci should have a greater impact in reducing the fitness of a polyploid population being inbred. This prediction can explain observations that homozygosities at different subchromosomal regions have distinct effects on inbreeding depression in polyploids. Furthermore, even mildly deleterious alleles can lead to large amounts of inbreeding depression because of their high equilibrium frequencies. Molecular studies correlating level of heterozygosity and degree of heterosis should take into account this nonuniform distribution of deleterious alleles in polyploid genomes. Preservation or enhancement of heterozygosity would be more critical at proximal regions than at other chromosome regions in polysomic polyploid species.

Alleles↗

A male-biased natal sex-ratio in inbred collared lemmings, Dicrostonyx groenlandicus.

A captive colony of collared lemmings (Dicrostonyx groenlandicus) from northern Alaska produced a male-biased sex ratio of 67% males for about three generations. These lemmings have a pair of autosomes fused to the sex chromosomes. Thus, males have two copies of some (formerly autosomal) sex-linked genes: One set is X-linked; the other can be described as Y-linked. Given such a karyotype, deleterious recessive alleles on the autosomal portion of the X chromosome are more resistant to selection than truly autosomal loci because they can be eliminated by homozygosity only in females. The male-bias could have resulted from one or more lethals carried on the formerly autosomal arm of the X chromosome. As inbreeding coefficients approached 0.3, the lethal was apparently homozygous in half of the homogametic (female) zygotes. This phenomenon may explain the excess of males and XY females attributed to meiotic drive in Dicrostonyx torquatus from Siberia. If under the natural mating system, inbreeding depression limits fitness, then fusion of autosomal chromatin to the sex chromosomes could be an adaptation to reduce inbreeding depression in heterogametic individuals.

Adaptation, Physiological↗

Mutation-selection balance accounting for genetic variation for viability in Drosophila melanogaster as deduced from an inbreeding and artificial selection experiment.

We carried out an experiment of inbreeding and upward artificial selection for egg-to-adult viability in a recently captured population of Drosophila melanogaster, as well as computer simulations of the experimental design, in order to obtain information on the nature of genetic variation for this important fitness component. The inbreeding depression was linear with a rate of 0.70 +/- 0.11% of the initial mean per 1% increase in inbreeding coefficient, and the realized heritability was 0.06 +/- 0.07. We compared the empirical observations of inbreeding depression and selection response with computer simulations assuming a balance between the occurrence of partially recessive deleterious mutations and their elimination by selection. Our results suggest that a model assuming mutation-selection balance with realistic mutational parameters can explain the genetic variation for viability in the natural population studied. Several mutational models are incompatible with some observations and can be discarded. Mutational models assuming a low rate of mutations of large average effect and highly recessive gene action, and others assuming a high rate of mutations of small average effect and close to additive gene action, are compatible with all the observations.

Animals↗

The effects of parasitism and inbreeding on the competitive ability in Daphnia magna: evidence for synergistic epistasis.

Synergistic epistasis for fitness is often assumed in models of how selection acts on the frequency and distribution of deleterious mutations. Evidence for synergistic epistasis would exist if the logarithm of fitness declines more quickly with number of deleterious mutations, than predicted by a linear decline. This can be studied indirectly by quantifying the effect of different levels of inbreeding on fitness. Here, six sets (different genetic backgrounds) of three increasingly inbred Daphnia magna clones were used to assess their relative fitness according to changes in frequency in a competition experiment against a tester clone. A novelty of the mating procedure was that the inbreeding coefficients (F) of the three clones belonging to each set increased in steps of 0.25 independent of the (unknown) inbreeding coefficient of the common ancestor. The equal increase of the inbreeding coefficients is important, because deviations influence the quantification of inbreeding depression, its variance and the detection of epistasis. In a simple mathematical model we show that when working with a partially inbred population inbreeding depression is underestimated, the variance of fitness is increased, and the detection of epistasis more difficult. Further, to examine whether an interaction between inbreeding and parasitism exists, each inbred clone was tested with and without a microsporidium infection (Octosporea bayeri). We found a nonlinear decrease of the logarithm of fitness across the three levels of inbreeding, indicating synergistic epistasis. The interaction term between parasitism and inbreeding was not significant. Our results suggest that deleterious mutations may be purged effectively once the level of inbreeding is high, but that parasitism seems not to influence this effect.

Animals↗

Conservation genetics.

Inbreeding depression, accumulation and loss of deleterious mutations, loss of genetic variation in small populations, genetic adaptation to captivity and its effect on reintroduction success, and outbreeding depression are reviewed. The impact of genetic factors in endangerment and extinction has been underestimated in some recent publications. Inbreeding depression in wildlife and in the field has been clearly established, while its impact has been greatly underestimated. The size of populations where genetic factors become important is higher than previously recognized, as Ne/N ratios average 0.11. Purging effects have been overestimated as a mechanism for eliminating deleterious alleles in small populations. The impact of loss of genetic variation in increasing the susceptibility of populations to environmental stochasticity and catastrophes has generally been ignored. Consequently, extinctions are often attributed to "nongenetic" factors when these may have interacted with genetic factors to cause extinction.

Adaptation, Biological↗

Family-level covariation between parasite resistance and mating system in a hermaphroditic freshwater snail.

Genetic compatibility, nonspecific defenses, and environmental effects determine parasite resistance. Host mating system (selfing vs. outcrossing) should be important for parasite resistance because it determines the segregation of alleles at the resistance loci and because inbreeding depression may hamper immune defenses. Individuals of a mixed mating hermaphroditic freshwater snail, Lymnaea ovata, are commonly infected by a digenetic trematode parasite, Echinoparyphium recurvatum. We examined covariation between quantitative resistance to novel parasites and mating system by exposing snail families from four populations that differed by their inbreeding coefficients. We found that resistance was unrelated to inbreeding coefficient of the population, suggesting that the more inbred populations did not carry higher susceptibility load than the less inbred populations. Most of the variation in resistance was expressed among the families within the populations. In the population with the lowest inbreeding coefficient, resistance increased with outcrossing rate of the family, as predicted if selfing had led to inbreeding depression. In the other three populations with higher inbreeding coefficients, resistance was unrelated to outcrossing rate. The results suggest that in populations with higher inbreeding some of the genetic load has been purged, uncoupling the predicted relationship between outcrossing rate and resistance. Snail families also displayed crossing reaction norms for resistance when tested in two environments that presented low and high immune challenge, suggesting that genotype-by-environment interactions are important for parasite resistance.

Animals↗

Effects of self-fertilization, environmental stress and exposure to xenobiotics on fitness-related traits of the freshwater snail Lymnaea stagnalis.

Genetic and ecological factors may interact in their effects on fitness. Such interactions are thus to be expected between inbreeding and exposure of a population to a toxicant. The magnitude of inbreeding depression is thought to increase in stressful environments. To test this hypothesis, we investigated the combined effects of environmental conditions and inbreeding on fitness in the self-fertile snail Lymnaea stagnalis, using a stress gradient (0-2) applied to a 100 isolated and paired lineages: laboratory control (0), outdoor microcosm control (1) and pesticide exposure under outdoor microcosm conditions (2). Outdoor stress conditions were maintained for 28 days prior to measurements of fitness traits (fecundity, hatching success, and size at hatching) under laboratory conditions, so that delayed environmental effects could be estimated. Under laboratory control conditions, we found significant initial family level heterogeneity for most measured traits, including physiological performances as assessed through energetic biomarkers. Whatever the environmental conditions, inbreeding depression was very low for progeny performances. Negative values of self-fertilization depression (SFD) were obtained. Unexpectedly, SFD showed a negative relationship with the assumed stress intensity, reflecting a higher sensitivity under pairing than under selfing, mostly due to parental fecundity. This suggests that stressful conditions may favour selfing. Stress intensity increased the distribution limits of both depression indices, suggesting that changes in fitness are less predictable in a population under stress. Implications of such findings for environmental risk assessment of pesticides are discussed.

Animals↗

Self-fertilization and the escape from pollen limitation in variable pollination environments.

Seed production in many plants is pollen limited, likely because of unpredictable variation in the pollinator environment. One way for plants to escape the consequences of pollinator variability is to evolve mating systems, such as autonomous selfing, that assure reproduction without relying on pollinators. We explore this hypothesis through the construction and analysis of heuristic models of plant population dynamics in seed- or site-limited populations. Our analysis suggests several important points: the familiar rule that inbreeding depression greater than 0.5 maintains outcrossing significantly underestimates the threshold required under pollen limited conditions with prior selfing; variability in the pollination environment erodes the ability of inbreeding depression to maintain outcrossing; and variable pollination environments can result in stable intermediate rates of prior selfing. The results reflect the importance of geometric mean fitness (which in a variable environment is less than the arithmetic mean) in the face of temporal variation.

Genetics, Population↗

Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data.

Geneticists have been interested in inbreeding and inbreeding depression since the time of Darwin. Two alternative approaches that can be used to measure how inbred an individual is involve the use of pedigree records to estimate inbreeding coefficients or molecular markers to measure multilocus heterozygosity. However, the relationship between inbreeding coefficient and heterozygosity has only rarely been investigated. In this paper, a framework to predict the relationship between the two variables is presented. In addition, microsatellite genotypes at 138 loci spanning all 26 autosomes of the sheep genome were used to investigate the relationship between inbreeding coefficient and multilocus heterozygosity. Multilocus heterozygosity was only weakly correlated with inbreeding coefficient, and heterozygosity was not positively correlated between markers more often than expected by chance. Inbreeding coefficient, but not multilocus heterozygosity, detected evidence of inbreeding depression for morphological traits. The relevance of these findings to the causes of heterozygosity--fitness correlations is discussed and predictions for other wild and captive populations are presented.

Animals↗

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.

Animals↗

Genetic diversity and reproductive success in mandrills (Mandrillus sphinx).

Recent studies of wild animal populations have shown that estimators of neutral genetic diversity, such as mean heterozygosity, are often correlated with various fitness traits, such as survival, disease susceptibility, or reproductive success. We used two estimators of genetic diversity to explore the relationship between heterozygosity and reproductive success in male and female mandrills (Mandrillus sphinx) living in a semifree ranging setting in Gabon. Because social rank is known to influence reproductive success in both sexes, we also examined the correlation between genetic diversity and social rank in females, and acquisition of alpha status in males, as well as length of alpha male tenure. We found that heterozygous individuals showed greater reproductive success, with both females and males producing more offspring. However, heterozygosity influenced reproductive success only in dominant males, not in subordinates. Neither the acquisition of alpha status in males, nor social rank in females, was significantly correlated with heterozygosity, although more heterozygous alpha males showed longer tenure than homozygous ones. We also tested whether the benefits of greater genetic diversity were due mainly to a genome-wide effect of inbreeding depression or to heterosis at one or a few loci. Multilocus effects best explained the correlation between heterozygosity and reproductive success and tenure, indicating the occurrence of inbreeding depression in this mandrill colony.

Animals↗

Reversed selection responses in small populations of the housefly (Musca domestica L.).

We compared the efficacy of artificial and natural selection processes in purging the genetic load of perpetually small populations. We subjected replicate lines of the housefly (Musca domestica L.), recently derived from the wild, to artificial selection for increased mating propensity (i.e., the proportion of male-female pairs initiating copulation within 30 min) in efforts to cull out the inbreeding depression effects of long-term small population size (as determined by a selection protocol for increased assortative mating). We also maintained parallel non-selection lines for assessing the spontaneous purge of genetic load due to inbreeding alone. We thus evaluated the fitness of artificially and 'naturally' purging populations held at census sizes of 40 individuals over the course of 18 generations. We found that the artificially selected lines had significant increases in mating propensity (up to 46% higher from the beginning of the protocol) followed by reversed selection responses back to the initial levels, resulting in non-significant heritabilities. Nevertheless, the 'naturally' selected lines had significantly lower fitness overall (a 28% reduction from the beginning of the protocol), although lower effective population sizes could have contributed to this effect. We conclude that artificial selection bolstered fitness, but only in the short-term, because the inadvertent fixation of extant genetic load later resulted in pleiotropic fitness declines. Still, the short-term advantage of the selection protocol likely contributed to the success of the speciation experiment since our recently-derived housefly populations are particularly vulnerable to inbreeding depression effects on mating behavior.

Animal Population Groups↗

Invasion dynamics of two alien Carpobrotus (Aizoaceae) taxa on a Mediterranean island: II. Reproductive strategies.

This study compares sexually and asexually produced fruit set, seed production, biomass, germination, and seedling size in Carpobrotus acinaciformis and C. edulis following controlled pollination experiments in order to evaluate the potential role of reproductive traits with respect to the invasive potential of these taxa. C. edulis is slightly agamospermic, completely self-fertile, slightly preferentially self-compatible, experiences no inbreeding depression, and has low hybrid vigour. In contrast, C. acinaciformis does not have reliable agamospermy, is only slightly self-fertile and self-compatible, experiences a slight inbreeding depression, and has a strong hybrid vigour. Both taxa have relatively low, although significantly different germination frequencies, and insignificantly different seedling sizes. Owing to the high performance in hybridisation as compared to all other controlled pollinations in C. acinaciformis, as well as a large amount of previously demonstrated introgression, we refer to the population studied on the island of Bagaud (France) as C. affine acinaciformis. We conclude that both C. edulis and C. affine acinaciformis should be considered as harmful invasive plants in the Mediterranean Basin, the former because of the flexibility of its mating system and high seed production, and the latter because of its strong clonality, high hybrid vigour, and potential for continued introgression from C. edulis genes. These differences require different control strategies, while the avoidance of sympatry is a distinct priority.

Aizoaceae↗

Exotic mice as models for aging research: polemic and prospectus by R. Miller et al.

Miller and colleagues present a polemic against uniform genotypes in gerontological research and a paean for genetically heterogeneous populations. Both on simple sampling considerations, and because of selective loss of alleles through inbreeding depression, inbred strains are idiosyncratic, and the lack of genetic variance within strains limits their utility in examining relationships among phenotypes. Heterogeneous stocks, by contrast, are not impaired by inbreeding depression, and the presence of genetic and environmental variance provides for effective assessment of correlations among variables. Those assembled by intermating of inbred strains are replicable in terms of gene pool parameters, even if no individual can ever be replicated, and those derived from wild-trapping may include alleles absent for whatever reason from current laboratory strains. This author concurs that there are limitations on research with uniform genotypes and advantages of heterogeneous populations. However, for specific purposes, the uniformity and stability of inbred strains are extremely valuable attributes, and heterogeneous stocks have their own limitations. Researchers should select the animal model most appropriate for their specific purpose.

Aging↗

Selection with partial selfing. I. Mass selection.

The expected responses to mass selection carried out before or after reproduction in a population whose members all have a fixed probability of self pollination (s) are formulated using covariances of relatives and their component quadratic functions for a model with arbitrary additive and dominance effects. The response measured in the first generation offspring after selection (immediate gain) can differ from that retained when the population has regained equilibrium (permanent gain). The population mean behaves in a predictable manner during the return to equilibrium, and its value at any time can be predicted from earlier generations. The permanent gain from selection after reproduction is always (1 + s)/2 times as large as that from selection before reproduction, but the relationship of the immediate gains depends on the genetic model assumed. Numerical analysis applied to a model with two alleles per locus and varying allele frequencies, dominance ratios and numbers of loci showed that the proportion of the immediate gain retained at equilibrium was reduced with the large inbreeding depression associated with increasing dominance levels and numbers of loci and was generally lower for selection after reproduction than before. In the absence of information as to the magnitude of genetic variances and inbreeding depression in species reproducing by partial selfing, the importance of this phenomenon is unknown.

Genetic Variation↗

Genetic cost of reproductive assurance in a self-fertilizing plant.

The transition from outcrossing to self-fertilization is one of the most common evolutionary trends in plants. Reproductive assurance, where self-fertilization ensures seed production when pollinators and/or potential mates are scarce, is the most long-standing and most widely accepted explanation for the evolution of selfing, but there have been few experimental tests of this hypothesis. Moreover, many apparently adaptive floral mechanisms that ensure the autonomous production of selfed seed might use ovules that would have otherwise been outcrossed. This seed discounting is costly if selfed offspring are less viable than their outcrossed counterparts, as often happens. The fertility benefit of reproductive assurance has never been examined in the light of seed discounting. Here we combine experimental measures of reproductive assurance with marker-gene estimates of self-fertilization, seed discounting and inbreeding depression to show that, during 2 years in 10 Ontario populations of Aquilegia canadensis (Ranunculaceae), reproductive assurance through self-fertilization increases seed production, but this benefit is greatly outweighed by severe seed discounting and inbreeding depression.

Fertility↗

The evolutionary genetics of sexual systems in flowering plants.

Population genetic studies of the evolution of breeding systems in flowering plants are reviewed. The selective advantage of a gene's increasing the selfing rate is stressed. In the evolution of outbreeding mechanisms, some strong disadvantage to selfing must therefore be acting; it is suggested that this disadvantage is inbreeding depression. Populations with no absolute barrier to selfing, and with intermediate levels of self-fertilization, appear to be the most likely starting state for the evolution of outbreeding mechanisms. There is some evidence for inbreeding depression in such populations. The evolution of distyly and dioecy are considered in some detail. An explanation for the existence of supergenes controlling these systems is proposed. The breakdown of distyly and tristyly are also considered. The evolution of recombination rates in selfing and outcrossing species is examined briefly.

Biological Evolution↗

Negative environmental perturbations may improve species persistence.

Among the factors proximally involved in the extinction of small isolated populations, genetic deterioration and temporal variation in environmental quality have been the subjects of intensive research in ecological and evolutionary sciences. However, previous theoretical studies and population viability assessments generally assumed a strict dichotomy between these two types of threat. Yet a number of empirical studies have recently suggested that the effects of genetic deterioration and environmental variation should not be considered independently, by demonstrating that the main effect of inbreeding depression lies with its tendency to exacerbate the deleterious consequences of environmental stress. Capitalizing on these results, I developed a stochastic model to examine the impact of random environmental perturbations on the persistence time of small isolated populations subject to inbreeding depression and mutation accumulation. The model assumes that spontaneous deleterious mutations have more severe effects when perturbations occur, which results in more efficient purging of the mutation load. Under this assumption, I find that negative perturbations may paradoxically improve middle- and long-term species persistence for realistic frequency of occurrence and severity distribution.

Animals↗