A new theory for the evolution of polyandry as a means of inbreeding avoidance

We propose a novel theory for the evolution of polyandry driven by genetic benefits to females whose offspring interbreed. In species with an ecology characterized by frequent colonization of new habitat patches, consanguineous matings may be common during the early stages of colonization, but genetic diversity may grow as new colonizers arrive. We show that with levels of inbreeding depression similar to those found in predominantly inbreeding populations, a polyandrous female can benefit her descendants since matings among her brood are mainly between half siblings rather than full siblings. We examine the invasion by a polyandrous phenotype using explicit genetic models in which costs of inbreeding are themselves subject to selection. In common with other models of inbreeding, we find that underlying high levels of inbreeding tend to purge deleterious recessive alleles, and hence these are unlikely to maintain sufficient inbreeding depression to favour polyandry. However, if costs of inbreeding are due to overdominance, biologically realistic levels of inbreeding depression result in genetic benefits large enough to favour polyandry provided it is not too costly. The potential significance of polyandry as a mechanism to reduce inbreeding in grandchildren will depend upon the genetic basis of inbreeding depression in natural, inbreeding populations.     

Theoretical aspects of extinction by inbreeding depression

Populational extinction due to inbreeding depression is analyzed with simple population genetic and population ecological models. Two alternative genetic mechanisms of inbreeding depression, i.e. recessive deleterious genes and overdominant genes, are assumed in separate analyses in order to examine their relative importance. With both mechanisms the population size and the coefficient of inbreeding are maintained at stable equilibria if there is no non-genetic demographic disturbance or stress. With a certain amount of demographic disturbance the population declines rapidly due to interaction between the decrease of population size and the increase of inbreeding coefficient. Such rapid extinction occurs with both genetic mechanisms. However, in the case of overdominant genes extinction happens only if the equilibrium population size is small and the selection coefficient is large such that segregation load is large. In nature, extinction due to overdominant genes is considered to be much less likely than extinction due to recessive deleterious genes.     

Family level inbreeding depression and the evolution of plant mating systems

Variation in the magnitude of inbreeding depression (ID) among families may have important consequences for mating system evolution. Experimental studies have shown that such variation is a common feature of natural plant populations. Unfortunately, the genetic and evolutionary significance of family level estimates remains obscure. Almost any kind of genetic variation will generate differences in ID among families, and as a consequence, a non-zero variance in family level ID is not sufficient to distinguish genetic architectures with wholly different implications for mating system evolution. Quantitative genetic methods provide a means to extract more information from ID experiments. Estimates of quantitative genetic variance components directly inform questions about the genetic basis of ID and should ultimately allow tests of alternative theories of mating system evolution.     

Effects of inbreeding on aversive learning in Drosophila

Inbreeding adversely affects life history traits as well as various other fitness‐related traits, but its effect on cognitive traits remains largely unexplored, despite their importance to fitness of many animals under natural conditions. We studied the effects of inbreeding on aversive learning (avoidance of an odour previously associated with mechanical shock) in multiple inbred lines of Drosophila melanogaster derived from a natural population through up to 12 generations of sib mating. Whereas the strongly inbred lines after 12 generations of inbreeding (0.75 < F < 0.93) consistently showed reduced egg‐to‐adult viability (on average by 28%), the reduction in learning performance varied among assays (average = 18% reduction), being most pronounced for intermediate conditioning intensity. Furthermore, moderately inbred lines (F = 0.38) showed no detectable decline in learning performance, but still had reduced egg‐to‐adult viability, which indicates that overall inbreeding effects on learning are mild. Learning performance varied among strongly inbred lines, indicating the presence of segregating variance for learning in the base population. However, the learning performance of some inbred lines matched that of outbred flies, supporting the dominance rather than the overdominance model of inbreeding depression for this trait. Across the inbred lines, learning performance was positively correlated with the egg‐to‐adult viability. This positive genetic correlation contradicts a trade‐off observed in previous selection experiments and suggests that much of the genetic variation for learning is owing to pleiotropic effects of genes affecting functions related to survival. These results suggest that genetic variation that affects learning specifically (rather than pleiotropically through general physiological condition) is either low or mostly due to alleles with additive (semi‐dominant) effects.     

Mating system and ploidy influence levels of inbreeding depression in Clarkia (Onagraceae)

Inbreeding depression is the reduction in offspring fitness associated with inbreeding and is thought to be one of the primary forces selecting against the evolution of self-fertilization. Studies suggest that most inbreeding depression is caused by the expression of recessive deleterious alleles in homozygotes whose frequency increases as a result of self-fertilization or mating among relatives. This process leads to the selective elimination of deleterious alleles such that highly selfing species may show remarkably little inbreeding depression. Genome duplication (polyploidy) has also been hypothesized to influence levels of inbreeding depression, with polyploids expected to exhibit less inbreeding depression than diploids. We studied levels of inbreeding depression in allotetraploid and diploid species of Clarkia (Onagraceae) that vary in mating system (each cytotype was represented by an outcrossing and a selfing species). The outcrossing species exhibited more inbreeding depression than the selfing species for most fitness components and for two different measures of cumulative fitness. In contrast, though inbreeding depression was generally lower for the polyploid species than for the diploid species, the difference was statistically significant only for flower number and one of the two measures of cumulative fitness. Further, we detected no significant interaction between mating system and ploidy in determining inbreeding depression. In sum, our results suggest that a taxon's current mating system is more important than ploidy in influencing levels of inbreeding depression in natural populations of these annual plants.     

Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana

The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter‐population crosses may therefore exhibit heterosis (increased fitness relative to intra‐population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs of Arabidopsis thaliana from 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (median F_ST = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.     

Environment-dependent inbreeding depression in a hermaphroditic freshwater snail

Inbreeding depression was simultaneously studied under contrasted environments, laboratory and natural conditions, using individuals originating from 14 families of the freshwater snail Physa acuta. Both survival and growth of juveniles showed inbreeding depression under laboratory conditions. The same fitness components were monitored with mature snails either kept under laboratory conditions or released at a natural site and analysed using capture-mark-recapture models. Genetic composition of both samples was similar. Inbreeding depression on survival was highest in the laboratory while strong outbreeding depression was revealed in the field. Thus inbreeding depression may not be always higher under natural conditions, at the opposite of what is commonly assumed. We suggest that inbreeding depression is dependent on metabolic requirements imposed by the environment. Other evidences showing that inbreeding depression is environment-dependent are reviewed. We conclude that genetic models should include both genetic and environmental variance in inbreeding depression for studying mating system evolution.     

Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa

Stressful environments are often said to increase the expression of inbreeding depression. Alternatively, Crow's "opportunity for selection" (the squared phenotypic coefficient of variation) sets a limit to how much selection can occur, constraining the magnitude of inbreeding depression. To test these hypotheses, we planted self- and cross-fertilized seeds of Brassica rapa into a factorial experiment that varied plant density and saline watering stresses. We then repeated the experiment, reducing the salt concentration. We observed considerable inbreeding depression, particularly for survival in the first experiment and growth in the second. Both stresses independently depressed plant performance. Families differed in their amounts of inbreeding depression and reaction norms across environments. Outcrossed progeny were sometimes more variable. Stresses had small and inconsistent effects on inbreeding depression and, when significant, tended to diminish it. Levels of phenotypic variability often predicted whether inbreeding depression would increase or decrease across environments and were particularly effective in predicting which traits display the most inbreeding depression. Thus, we find little support for the stress hypothesis and mixed support for the phenotypic variability hypothesis. Variable levels of phenotypic variation provide a parsimonious explanation for shifts in inbreeding depression that should be tested before invoking more complex hypotheses.     

Inbreeding depression: tests of the overdominance and partial dominance hypotheses

The two principal theories of the causal mechanism for inbreeding depression are the partial dominance hypothesis and the overdominance hypothesis. According to the first hypothesis, inbreeding increases the frequency of homozygous combinations of deleterious recessive alleles thereby decreasing fitness, whereas the overdominance hypothesis posits that inbreeding increases homozygosity and thus reduces the frequency of the superior heterozygotes. These two hypotheses make different predictions on the effect of crossing inbred lines: the overdominance hypothesis predicts that trait means will be restored to the outbred means, whereas the partial dominance hypothesis predicts that trait means will exceed those of the outbred population. I tested these predictions using seven inbred lines of the sand cricket, Gryllus firmus. Fourteen generations of brother-sister mating resulted in an inbreeding depression of 20-34% in four traits: nymphal weights at ages 14 days, 21 days, 28 days, and early fecundity. An incomplete diallel cross of these lines showed genetic variation among lines and an increase in all trait means above the outbred means, with three being significantly higher. These results provide support for the partial dominance hypothesis and are inconsistent with the overdominance hypothesis.     

Inbreeding depression in the competitive fertilization success of male crickets

Mating between close relatives generally results in offspring of decreased fitness. Inbreeding depression is generally greater for life-history traits than for morphological traits, and recent studies of traits subject to sexual selection suggest that these may suffer the greatest inbreeding depression. Sexual selection continues after mating in the form of sperm competition and cryptic female choice, imposing strong selection on male competitive fertilization success. Here, I examine the effects of a single generation of full-sib mating on competitive fertilization success in a cricket, Teleogryllus oceanicus. The estimated coefficient of inbreeding depression in competitive fertilization success was 0.37, higher than that for other life-history and morphological traits. Such intense inbreeding depression coupled with little or no additive genetic variance for this trait is consistent with strong directional selection on male competitive fertilization success generating high levels of dominance variance, and provides an adaptive explanation for the evolution of inbreeding avoidance found in this species.     

Population type can influence the magnitude of inbreeding depression in Clarkia concinna (Onagraceae)

Fragmented populations may face high risk of extinction due to the deleterious consequences of increased inbreeding or of genetic drift in small and isolated populations. Theories on the mechanisms of inbreeding depression predict that the severity of inbreeding depression can eventually decrease in populations that persistently inbreed, and hence populations that are isolated through habitat fragmentation might experience a decrease in inbreeding depression over time. In this study, we tested this hypothesis using the patchily distributed, outcrossing annual plant, Clarkia concinna concinna (Onagraceae), which naturally experiences many fragmentation effects. We collected seeds from isolated and central subpopulations and created artificially inbred and outcrossed lines. Progeny from these crosses were planted into the field and greenhouse and assayed for fitness traits over the course of a growing season. Overall, inbreeding depression was substantial, ranging as high as 0.76 (for cumulative fitness in the field), and significant for plant height, fecundity, and above-ground biomass in all experiments. No inbreeding depression was detected for germination or survival rates in the greenhouse experiments, but in the field, survival was significantly depressed for inbred progeny. There was no evidence to support our hypothesis that increased inbreeding in isolated populations would lead to the purging of deleterious alleles and a decrease in the severity inbreeding depression. The most likely hypothesis to explain our results is that purging is not occurring more strongly in the isolated populations due to details of a number of genetic factors (e.g., selection against deleterious alleles is inconsistent or insufficient, or drift has caused fixation of deleterious alleles in these populations). This study supports the view that even when inbreeding depression is predicted to be less problematic, it may still be an important force influencing the fitness of populations. This revised version was published online in July 2006 with corrections to the Cover Date.     

Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging

An important issue in conservation biology and the study of evolution is the extent to which inbreeding depression can be reduced or reversed by natural selection. If the deleterious recessive alleles causing inbreeding depression can be 'purged' by natural selection, outbred populations that have a history of inbreeding are expected to be less susceptible to inbreeding depression. This expectation, however, has not been realized in previous laboratory experiments. In the present study, we used Drosophila melanogaster as a model system to test for an association between inbreeding history and inbreeding depression. We created six 'purged' populations from experimental lineages that had been maintained at a population size of 10 male-female pairs for 19 generations. We then measured the inbreeding depression that resulted from one generation of full-sib mating in the purged populations and in the original base population. The magnitude of inbreeding depression in the purged populations was approximately one-third of that observed in the original base population. In contrast to previous laboratory experiments, therefore, we found that inbreeding depression was reduced in populations that have a history of inbreeding. The large purging effects observed in this study may be attributable to the rate of historical inbreeding examined, which was slower than that considered in previous experiments.     

The decline in fitness with inbreeding: evidence for negative dominance‐by‐dominance epistasis in Drosophila melanogaster

Genetic interactions can play an important role in the evolution of reproductive strategies. In particular, negative dominance‐by‐dominance epistasis for fitness can theoretically favour sex and recombination. This form of epistasis can be detected statistically because it generates nonlinearity in the relationship between fitness and inbreeding coefficient. Measures of fitness in progressively inbred lines tend to show limited evidence for epistasis. However, tests of this kind can be biased against detecting an accelerating decline due to line losses at higher inbreeding levels. We tested for dominance‐by‐dominance epistasis in Drosophila melanogaster by examining viability at five inbreeding levels that were generated simultaneously, avoiding the bias against detecting nonlinearity that has affected previous studies. We find an accelerating rate of fitness decline with inbreeding, indicating that dominance‐by‐dominance epistasis is negative on average, which should favour sex and recombination.     

Comparing the van Oosterhout and Chybicki‐Burczyk methods of estimating null allele frequencies for inbred populations

In spite of the usefulness of codominant markers in population genetics, the existence of null alleles raises challenging estimation issues in natural populations that are characterized by positive inbreeding coefficients (F > 0). Disregarding the possibility of F > 0 in a population will generally lead to overestimates of null allele frequencies. Conversely, estimates of inbreeding coefficients (F) may be strongly biased upwards (excess homozygotes), in the presence of nontrivial frequencies of null alleles. An algorithm has been presented for the estimation of null allele frequencies in inbred populations (van Oosterhout method), using external estimates of the F‐statistics. The goal of this study is to introduce a modification of this method and to provide a formal comparison with an alternative likelihood‐based method (Chybicki‐Burczyk). Using simulated data, we illustrate the strengths and limitations of these competing methods. Under most circumstances, the likelihood method is preferable, but for highly inbred organisms, a modified van Oosterhout method offers some advantages.     

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.     

Molecular and pedigree measures of relatedness provide similar estimates of inbreeding depression in a bottlenecked population

Individual‐based estimates of the degree of inbreeding or parental relatedness from pedigrees provide a critical starting point for studies of inbreeding depression, but in practice wild pedigrees are difficult to obtain. Because inbreeding increases the proportion of genomewide loci that are identical by descent, inbreeding variation within populations has the potential to generate observable correlations between heterozygosity measured using molecular markers and a variety of fitness related traits. Termed heterozygosity‐fitness correlations (HFCs), these correlations have been observed in a wide variety of taxa. The difficulty of obtaining wild pedigree data, however, means that empirical investigations of how pedigree inbreeding influences HFCs are rare. Here, we assess evidence for inbreeding depression in three life‐history traits (hatching and fledging success and juvenile survival) in an isolated population of Stewart Island robins using both pedigree‐ and molecular‐derived measures of relatedness. We found results from the two measures were highly correlated and supported evidence for significant but weak inbreeding depression. However, standardized effect sizes for inbreeding depression based on the pedigree‐based kin coefficients (k) were greater and had smaller standard errors than those based on molecular genetic measures of relatedness (RI), particularly for hatching and fledging success. Nevertheless, the results presented here support the use of molecular‐based measures of relatedness in bottlenecked populations when information regarding inbreeding depression is desired but pedigree data on relatedness are unavailable.     

Heterosis and inbreeding depression in bottlenecked populations: a test in the hermaphroditic freshwater snail Lymnaea stagnalis

Small population size is expected to induce heterosis, due to the random fixation and accumulation of mildly deleterious mutations, whereas within‐population inbreeding depression should decrease due to increased homozygosity. Population bottlenecks, although less effective, may have similar consequences. We tested this hypothesis in the self‐fertile freshwater snail Lymnaea stagnalis, by subjecting experimental populations to a single bottleneck of varied magnitude. Although patterns were not strong, heterosis was significant in the most severely bottlenecked populations, under stressful conditions. This was mainly due to hatching rate, suggesting that early acting and highly deleterious alleles were involved. Although L. stagnalis is a preferential outcrosser, inbreeding depression was very low and showed no clear relationship with bottleneck size. In the less reduced populations, inbreeding depression for hatching success increased under high inbreeding. This may be consistent with the occurence of synergistic epistasis between fitness loci, which may contribute to favour outcrossing in L. stagnalis.     

Environmental dependence of inbreeding depression and purging in Drosophila melanogaster

Elimination or reduction of inbreeding depression by natural selection at the contributing loci (purging) has been hypothesized to effectively mitigate the negative effects of inbreeding in small isolated populations. This may, however, only be valid when the environmental conditions are relatively constant. We tested this assumption using Drosophila melanogaster as a model organism. By means of chromosome balancers, chromosomes were sampled from a wild population and their viability was estimated in both homozygous and heterozygous conditions in a favourable environment. Around 50% of the chromosomes were found to carry a lethal or sublethal mutation, which upon inbreeding would cause a considerable amount of inbreeding depression. These detrimentals were artificially purged by selecting only chromosomes that in homozygous condition had a viability comparable to that of the heterozygotes (quasi-normals), thereby removing most deleterious recessive alleles. Next, these quasi-normals were tested both for egg-to-adult viability and for total fitness under different environmental stress conditions: high-temperature stress, DDT stress, ethanol stress, and crowding. Under these altered stressful conditions, particularly for high temperature and DDT, novel recessive deleterious effects were expressed that were not apparent under control conditions. Some of these chromosomes were even found to carry lethal or near-lethal mutations under stress. Compared with heterozygotes, homozygotes showed on average 25% additional reduction in total fitness. Our results show that, except for mutations that affect fitness under all environmental conditions, inbreeding depression may be due to different loci in different environments. Hence purging of deleterious recessive alleles can be effective only for the particular environment in which the purging occurred, because additional load will become expressed under changing environmental conditions. These results not only indicate that inbreeding depression is environment dependent, but also that inbreeding depression may become more severe under changing stressful conditions. These observations have significant consequences for conservation biology.     

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.     

A population dynamics model for annual plants subject to inbreeding depression

Summary We present a population dynamics model for annual plants subject to density dependent competition and a decline in mean individual fitness with inbreeding. An analysis of this model provides three distinct sets of parameter values that define the relative influence of inbreeding depression and density on population growth. First, a population with a relatively high finite rate of increase and a relatively small environmental carrying capacity can persist in spite of low levels of inbreeding depression. These types of population may occur during a bottleneck event that is caused by pure predation (or collecting) pressure rather than loss of habitat. Second, there can exist a minimum viable population size when the finite rate of increase is relatively low and the population is also affected by density: the growth or decline of the population will depend on the initial population size. Third, when the population is small enough to be simultaneously effected by density and by inbreeding depression, there can be no viable population.