The effects of migration load,selfing, inbreeding depression,and the genetics of adaptation on autotetraploid versus diploid establishment in peripheral habitats

The distribution and abundance of polyploids has intrigued biologists since their discovery in the early 20th century. A pattern in nature that may give insight to processes that shape the distribution and abundance of polyploids is that polyploid populations are sometimes associated with peripheral habitats within the range of a species of mixed ploidy. Here, adaptation and competition of a diploid versus an autotetraploid population in a peripheral habitat are examined theoretically. It is shown that a nascent autotetraploid population adapts to and outcompetes a diploid population in the periphery when the rate of gamete dispersal is high, and when the mode of gene action is recessive for moderate to high rates of selfing. With additive or dominant modes of gene action, the conditions for an autotetraploid to outcompete a diploid in the periphery appear determined more by the rate of selfing and less by gamete dispersal. All of these results are based on empirical work that suggests inbreeding depression is higher in diploids versus autotetraploids. Generally, the results indicate that, although autotetraploids incur minority cytotype exclusion, diploids face burdens themselves. In the case of adaptation to a peripheral habitat, this burden is migration load from gamete and propagule dispersal.     

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.     

Effects of population size and metapopulation dynamics on a mating-system polymorphism

The evolutionary dynamics of neutral alleles under the Wright-Fisher model are well understood. Similarly, the effect of population turnover on neutral genetic diversity in a metapopulation has attracted recent attention in theoretical studies. Here we present the results of computer simulations of a simple model that considers the effects of finite population size and metapopulation dynamics on a mating-system polymorphism involving selfing and outcrossing morphs. The details of the model are based on empirical data from dimorphic populations of the annual plant Eichhornia paniculata, but the results are also of relevance to species with density-dependent selfing rates in general. In our model, the prior selfing rate is determined by two alleles segregating at a single diploid locus. After prior selfing occurs, some remaining ovules are selfed through competing self-fertilisation in finite populations as a result of random mating among gametes. Fitness differences between the mating-system morphs were determined by inbreeding depression and pollen discounting in a context-dependent manner. Simulation results showed evidence of frequency dependence in the action of pollen discounting and inbreeding depression in finite populations. In particular, as a result of selfing in outcrossers through random mating among gametes, selfers experienced a "fixation bias" through drift, even when the mating-system locus was selectively neutral. In a metapopulation, high colony turnover generally favoured the fixation of the outcrossing morph, because inbreeding depression reduced opportunities for colony establishment by selfers through seed dispersal. Our results thus demonstrate that population size and metapopulation processes can lead to evolutionary dynamics involving pollen and seed dispersal that are not predicted for large populations with stable demography.     

Outcrossing rate and inbreeding depression in the herbaceous autotetraploid,Campanula americana

Polyploidy in angiosperms is frequently associated with an increase in self-compatibility. Self-fertilization can enhance polyploid establishment, and theory predicts reduced inbreeding depression in polyploids relative to diploids. Therefore, we may expect mating systems that promote self-fertilization or mixed-mating in polyploid species. However, few studies have measured polyploid mating systems and inbreeding depression. We report the outcrossing rate and inbreeding depression for Campanula americana, a self-compatible protandrous herb. Allozyme genotypes suggest that C. americana is an autotetraploid with tetrasomic inheritance. We found that the multilocus outcrossing rate, t(m)=0.938, did not differ from unity. This result was unexpected since previous work demonstrated that pollinators frequently move from male- to female-phase flowers on the same plant, that is, geitonogamy. Self and outcross pollinations were conducted for three populations. Offspring were germinated in controlled conditions and grown to maturity in pots in nature. Inbreeding depression was not significant for most seed and germination characters. However, all later life traits except flowering date differed between inbred and outcrossed individuals resulting in a 26% reduction in cumulative fitness for inbred plants. Limited early- and moderate later-life inbreeding depression suggest that it is buffered by the higher levels of heterozygosity found in an autotetraploid. C. americana appears to have a flexible mating system where within flower protandry and/or cryptic self-incompatibility result in a high outcrossing rate when pollinators are abundant, but self-compatibility and limited inbreeding depression maintain reproductive success when mates are limited.     

Individual Variation in Inbreeding Depression: The Roles of Inbreeding History and Mutation

We use mutation-selection recursion models to evaluate the relative contributions of mutation and inbreeding history to variation among individuals in inbreeding depression and the ability of experiments to detect associations between individual inbreeding depression and mating system genotypes within populations. Poisson mutation to deleterious additive or recessive alleles generally produces far more variation among individuals in inbreeding depression than variation in history of inbreeding, regardless of selfing rate. Moreover, variation in inbreeding depression can be higher in a completely outcrossing or selfing population than in a mixed-mating population. In an initially random mating population, the spread of a dominant selfing modifier with no pleiotropic effects on male outcross success causes a measurable increase in inbreeding depression variation if its selfing rate is large and inbreeding depression is caused by recessive lethals. This increase is observable during a short period as the modifier spreads rapidly to fixation. If the modifier alters selfing rate only slightly, it fails to spread or causes no measurable increase in inbreeding depression variance. These results suggest that genetic associations between mating loci and inbreeding depression loci could be difficult to demonstrate within populations and observable only transiently during rapid evolution to a substantially new selfing rate.     

Neopolyploidy and diversification in Heuchera grossulariifolia

Newly formed polyploid lineages must contend with several obstacles to avoid extinction, including minority cytotype exclusion, competition, and inbreeding depression. If polyploidization results in immediate divergence of phenotypic characters these hurdles may be reduced and establishment made more likely. In addition, if polyploidization alters the phenotypic and genotypic associations between traits, that is, the P and G matrices, polyploids may be able to explore novel evolutionary paths, facilitating their divergence and successful establishment. Here, we report results from a study of the perennial plant Heuchera grossulariifolia in which the phenotypic divergence and changes in phenotypic and genotypic covariance matrices caused by neopolyploidization have been estimated. Our results reveal that polyploidization causes immediate divergence for traits relevant to establishment and results in significant changes in the structure of the phenotypic covariance matrix. In contrast, our results do not provide evidence that polyploidization results in immediate and substantial shifts in the genetic covariance matrix.     

Inbreeding depression is high in a self‐incompatible perennial herb population but absent in a self‐compatible population showing mixed mating

High inbreeding depression is thought to be one of the major factors preventing evolutionary transitions in hermaphroditic plants from self‐incompatibility (SI) and outcrossing toward self‐compatibility (SC) and selfing. However, when selfing does evolve, inbreeding depression can be quickly purged, allowing the evolution of complete self‐fertilization. In contrast, populations that show intermediate selfing rates (a mixed‐mating system) typically show levels of inbreeding depression similar to those in outcrossing species, suggesting that selection against inbreeding might be responsible for preventing the transition toward complete self‐fertilization. By implication, crosses among populations should reveal patterns of heterosis for mixed‐mating populations that are similar to those expected for outcrossing populations. Using hand‐pollination crosses, we compared levels of inbreeding depression and heterosis between populations of Linaria cavanillesii (Plantaginaceae), a perennial herb showing contrasting mating systems. The SI population showed high inbreeding depression, whereas the SC population displaying mixed mating showed no inbreeding depression. In contrast, we found that heterosis based on between‐population crosses was similar for SI and SC populations. Our results are consistent with the rapid purging of inbreeding depression in the derived SC population, despite the persistence of mixed mating. However, the maintenance of outcrossing after a transition to SC is inconsistent with the prediction that populations that have purged their inbreeding depression should evolve toward complete selfing, suggesting that the transition to SC in L. cavanillesii has been recent. SC in L. cavanillesii thus exemplifies a situation in which the mating system is likely not at an equilibrium with inbreeding depression.     

Effect of recurrent selfing on inbreeding depression and mating system evolution in an autopolyploid plant

Genome duplication resulting in polyploidy can have significant consequences for the evolution of mating systems. Most theory predicts that self‐fertilization will be selectively favored in polyploids; however, many autopolyploids are outcrossing or mixed‐mating. Here, we examine the hypothesis that the evolution of selfing is restricted in autopolyploids because the genetic cost of selfing (i.e., inbreeding depression) increases monotonically with successive generations of inbreeding. Using the herbaceous, autotetraploid plant Chamerion angustifolium, we generated populations with different inbreeding coefficients (F= 0, 0.17 and 0.36) through three consecutive generations of selfing and compared their magnitudes of inbreeding depression in a common environment. Mating system estimates for four natural populations confirmed that tetraploid selfing rates (s_m= 0.25, SE = 0.02) are similar to those of diploids (s_m= 0.12, SE = 0.12; F_1,2= 1.34, P= 0.37) indicating that both cytotypes are predominantly outcrossing. Compared to an outbred control line, mean inbreeding depression for seed production, survival, and height (vegetative and total) in the inbred line differed among generations (inbreeding coefficients). Across all stages, inbreeding depression (relative to control) was positively related to generation (inbreeding coefficient). Although the initial costs of inbreeding in extant and newly synthesized polyploids may be low compared to diploids, the monotonic increase in inbreeding depression with repeated inbreeding may limit the extent to which selfing variants are favored.     

Estimating Long-Term Mating Systems Using DNA Sequences

Plant mating systems often involve a mixture of self fertilizations and outcross fertilizations. The degree of selfing has a large impact on the genetic composition of natural populations and on the evolution of the mating system itself in response to such factors as inbreeding depression. This paper describes a means of estimating the long-term rate of self-fertilization from samples of alleles taken from individuals in a population. Use is made of the genealogy of pairs of alleles at a locus within individuals and pairs between individuals. The degree of selfing is closely related to the extent to which the number of nucleotide sites differing within an individual is reduced relative to the number differing between individuals. Importantly, the estimate of long-term selfing is largely independent of population size and is not affected by historical fluctuations in population size; instead it responds directly to the mating system itself. The approach outlined here is most appropriate to evolutionary problems in which the long-term nature of the mating system is of interest, such as to determine the relationship between prior inbreeding and inbreeding depression.     

Variability of individual genetic load: consequences for the detection of inbreeding depression

Inbreeding depression is a key factor affecting the persistence of natural populations, particularly when they are fragmented. In species with mixed mating systems, inbreeding depression can be estimated at the population level by regressing the average progeny fitness by the selfing rate of their mothers. We applied this method using simulated populations to investigate how population genetic parameters can affect the detection power of inbreeding depression. We simulated individual selfing rates and genetic loads from which we computed fitness values. The regression method yielded high statistical power, inbreeding depression being detected as significant (5?% level) in 92?% of the simulations. High individual variation in selfing rate and high mean genetic load led to better detection of inbreeding depression while high among-individual variation in genetic load made it more difficult to detect inbreeding depression. For a constant sampling effort, increasing the number of progenies while decreasing the number of individuals per progeny enhanced the detection power of inbreeding depression. We discuss the implication of among-mother variability of genetic load and selfing rate on inbreeding depression studies.     

A unified model of autopolyploid establishment and evolution

The prevalence of polyploidy among flowering plants is surprising given the hurdles impeding the establishment and persistence of novel polyploid lineages. In the absence of strong assortative mating, reproductive assurance, or large intrinsic fitness advantages, new polyploid lineages face almost certain extinction through minority cytotype exclusion. Consequently, much work has focused on a search for adaptive advantages associated with polyploidy such as increased competitive ability, enhanced ecological tolerances, and increased resistance to pathogens. Yet, no consistent adaptive advantages of polyploidy have been identified. Here, to investigate the potential for autopolyploid establishment and persistence in the absence of any intrinsic fitness advantages, we develop a simulation model of a diploid population that sporadically gives rise to novel autopolyploids. The autopolyploids have only very small levels of initial assortative mating or niche differentiation, generated entirely by dosage effects of genome duplication, and they have realistic levels of reproductive assurance. Our results show that by allowing assortative mating and competitive interactions to evolve, establishment of novel autopolyploid lineages becomes common. Additional scenarios where adaptive optima change over time reveal that rapid environmental change promotes the replacement of diploid lineages by their autopolyploid descendants. These results help to explain recent empirical findings that suggest that many contemporary polyploid lineages arose during the Cretaceous-Tertiary extinction, without invoking adaptive advantages of polyploidy.     

The cost of fluctuating inbreeding depression

We present a phenotypic model for the evolution of self-fertilization in an infinite population of annual hermaphrodites for the case in which fitness and inbreeding depression vary among generations (e.g., due to fluctuations in the environment from year to year). Conditions for the evolution of selfing, mixed mating, and outcrossing are derived and are compared with results from numerical calculations that assume a normal distribution of inbreeding depression. In contrast to the situation in which inbreeding depression does not vary, when inbreeding depression fluctuates in a stochastic manner among generations with a mean less than 0.5, selfing is not necessarily selected. Thus, fluctuating inbreeding depression can be viewed as an additional cost of selfing that may stabilize mixed mating systems. These results emphasize the need to take into account fluctuating inbreeding depression in empirical studies aimed at understanding mating system evolution in annuals.     

Increased inbreeding but not homozygosity in small populations of Sabatia angularis (Gentianaceae)

Understanding how the mating system varies with population size in plant populations is critical for understanding their genetic and demographic fates. We examined how the mating system, characterized by outcrossing rate, biparental inbreeding rate, and inbreeding coefficient, and genetic diversity varied with population size in natural populations of the biennial Sabatia angularis. We found a significant, positive relationship between outcrossing and population size. Selfing was as high as 40% in one small population but was only 7% in the largest population. Despite this pattern, observed heterozygosity did not vary with population size, and we suggest that selection against inbred individuals maintains observed heterozygosity in small populations. Consistent with this hypothesis, we found a trend of lower inbreeding coefficients in the maternal than progeny generation in all of the populations, and half of the populations exhibited significant excesses of adult heterozygosity. Moreover, genetic diversity was not related to population size and was similar across all populations examined. Our results suggest that the consequences of increased selfing for population fitness in S. angularis, a species that experiences significant inbreeding depression, will depend on the relative magnitude and consistency of inbreeding depression and the demographic cost of selection for outcrossed progeny in small populations.     

Aneuploidy and inbreeding depression in random mating and self-fertilizing autotetraploid populations

Summary Almost all autotetraploids produce aneuploid progeny because of irregularities at meiosis. Aneuploid plants produce high frequencies of aneuploids. If it were not for selection against aneuploid gametes and sporophytes the amount of aneuploidy would increase every generation. Most experimental and theoretical studies on population genetics and heterosis in autotetraploids have neglected aneuploidy as a factor. To take aneuploidy into account experimentally requires the cytological identification of all chromosomes and to consider it theoretically requires a huge amount of computations. Consequently, microcomputer programs have been devised to show the effects of random mating and self-fertilization in autotetraploid populations. According to the model aneuploidy rapidly increases in randomly mated and self-fertilized autotetraploid populations until they achieve an equilibrium where the amount of aneuploidy introduced into the population is balanced by the amount of aneuploidy removed from the population by selection. The model suggests that self-fertilized populations have greater frequencies of aneuploid gametes and zygotes than do randomly mated populations and therefore aneuploidy may be a significant cause of the great inbreeding depressions found in autotetraploids.Contribution from the Missouri Agricultural Experiment Station. Journal Series No. 9998     

No correlation between inbreeding depression and delayed selfing in the freshwater snail Physa acuta

Inbreeding depression, one of the main factors driving mating system evolution, can itself evolve as a function of the mating system (the genetic purging hypothesis). Classical models of coevolution between mating system and inbreeding depression predict negative associations between inbreeding depression and selfing rate, but more recent approaches suggest that negative correlations should usually be too weak or transient to be detected within populations. Empirical results remain unclear and restricted to plants. Here, we evaluate, for the first time, the within-population genetic correlation between inbreeding depression and a trait that controls the amount of self-fertilization (the waiting time) in a self-fertile hermaphroditic animal, the freshwater snail Physa acuta. Using a large quantitative-genetic design (36 grand-families and 348 families), we observe abundant within-population family-level genetic variation for both inbreeding depression (estimated for survival, fecundity, and size) and the degree of behavioral selfing avoidance. However, we detected no correlation between waiting time and inbreeding depression across families. In agreement with recent models, this result shows that mutational variance rather than differential purging accounts for most of the genetic variance in inbreeding depression within a population.     

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.     

Functional pleiotropy and mating system evolution in plants: frequency-independent mating

Mutations that alter the morphology of floral displays (e.g., flower size) or plant development can change multiple functions simultaneously, such as pollen export and selfing rate. Given the effect of these various traits on fitness, pleiotropy may alter the evolution of both mating systems and floral displays, two characters with high diversity among angiosperms. The influence of viability selection on mating system evolution has not been studied theoretically. We model plant mating system evolution when a single locus simultaneously affects the selfing rate, pollen export, and viability. We assume frequency-independent mating, so our model characterizes prior selfing. Pleiotropy between increased viability and selfing rate reduces opportunities for the evolution of pure outcrossing, can favor complete selfing despite high inbreeding depression, and notably, can cause the evolution of mixed mating despite very high inbreeding depression. These results highlight the importance of pleiotropy for mating system evolution and suggest that selection by nonpollinating agents may help explain mixed mating, particularly in species with very high inbreeding depression.     

Mitosis, stature and evolution of plant mating systems: low-Phi and high-Phi plants

There is a long-recognized association in plants between small stature and selfing, and large stature and outcrossing. Inbreeding depression is central to several hypotheses for this association, but differences in the evolutionary dynamics of inbreeding depression associated with differences in stature are rarely considered. Here, we propose and test the Phi model of plant mating system evolution, which assumes that the per-generation mutation rate of a plant is a function of the number of mitoses (Phi) that occur from zygote to gamete, and predicts fundamental differences between low-Phi (small-statured) and high-Phi (large-statured) plants in the outcomes of the joint evolution of outcrossing rate and inbreeding depression. Using a large dataset of published population genetic studies of angiosperms and conifers, we compute fitted values of inbreeding depression and deleterious mutation rates for small- and large-statured plants. Consistent with our Phi model, we find that populations of small-statured plants exhibit a range of mating systems, significantly lower mutation rates, and intermediate inbreeding depression, while large-statured plants exhibit very high mutation rates and the maximum inbreeding depression of unity. These results indicate that (i) inbred progeny typically observed in large-statured plant populations are completely lost prior to maturity in nearly all populations; (ii) evolutionary shifts from outcrossing to selfing are generally not possible in large-statured species, rather, large-statured species are more likely to evolve mating systems that avoid selfing such as self-incompatibility and dioecy; (iii) destabilization of the mating system-high selfing rate with high-inbreeding depression-might be a common occurrence in large-statured species; and (iv) large-statured species in fragmented populations might be at higher risk of extinction than previously thought. Our results help to unify and simplify a large and diverse field of research, and serve to emphasize the importance that developmental and genetic constraints play in the evolution of plant mating systems.     

Reproductive compensation in the evolution of plant mating systems

Reproductive compensation, the replacement of dead embryos by potentially viable ones, is known to play a major role in the maintenance of deleterious mutations in mammalian populations. However, it has received little attention in plant evolution. Here we model the joint evolution of mating system and inbreeding depression with reproductive compensation. We used a dynamic model of inbreeding depression, allowing for partial purging of recessive lethal mutations by selfing. We showed that reproductive compensation tended to increase the mean number of lethals in a population, but favored self-fertilization by effectively decreasing early inbreeding depression. When compensation depended on the selfing rate, stable mixed mating systems can occur, with low to intermediate selfing rates. Experimental evidence of reproductive compensation is required to confirm its potential importance in the evolution of plant mating systems. We suggest experimental methods to detect reproductive compensation.     

THE EVOLUTION OF SELF-FERTILIZATION AND INBREEDING DEPRESSION IN PLANTS. I. GENETIC MODELS

The amounts of inbreeding depression upon selfing and of heterosis upon outcrossing determine the strength of selection on the selfing rate in a population when this evolves polygenically by small steps. Genetic models are constructed which allow inbreeding depression to change with the mean selfing rate in a population by incorporating both mutation to recessive and partially dominant lethal and sublethal alleles at many loci and mutation in quantitative characters under stabilizing selection. The models help to explain observations of high inbreeding depression (> 50%) upon selfing in primarily outcrossing populations, as well as considerable heterosis upon outcrossing in primarily selfing populations. Predominant selfing and predominant outcrossing are found to be alternative stable states of the mating system in most plant populations. Which of these stable states a species approaches depends on the history of its population structure and the magnitude of effect of genes influencing the selfing rate.