ON THE EVOLUTION OF PARTHENOGENESIS. II. INBREEDING AND THE COST OF MEIOSIS

Quantitative models of genetic change were analyzed to study the effect of inbreeding on the conditions for the evolution of parthenogenesis. Although inbreeding has been proposed as a key factor that may resolve the apparent paradox between the success of biparental reproduction and the genetic advantages of uniparental reproduction, the results indicate that inbreeding does not greatly change the cost of meiosis in diploids and actually increases it in haplodiploids. Inbreeding increases parent-offspring relatedness and the reproductive value of females. These direct effects act antagonistically on the cost of meiosis: higher relatedness between parents and biparentally-derived offspring promotes biparental reproduction, and high reproductive value of females promotes thelytoky. In diploids the two effects cancel one another, while in haplodiploids the latter predominates. A survey by Hamilton (1967) showed that a high proportion of haplodiploid species that undergo close inbreeding have thelytokous relatives, an association that is consistent with the result obtained here that, apart from its effect on the sex ratio, inbreeding directly promotes parthenogenesis in haplodiploids.     

EVOLUTION OF THE MAGNITUDE AND TIMING OF INBREEDING DEPRESSION IN PLANTS

Estimates of inbreeding depression obtained from the literature were used to evaluate the association between inbreeding depression and the degree of self-fertilization in natural plant populations. Theoretical models predict that the magnitude of inbreeding depression will decrease with inbreeding as deleterious recessive alleles are expressed and purged through selection. If selection acts differentially among life history stages and deleterious effects are uncorrelated among stages, then the timing of inbreeding depression may also evolve with inbreeding. Estimates of cumulative inbreeding depression and stage-specific inbreeding depression (four stages: seed production of parent, germination, juvenile survival, and growth/reproduction) were compiled for 79 populations (using means of replicates, N = 62) comprising 54 species from 23 families of vascular plants. Where available, data on the mating system also were collected and used as a measure of inbreeding history. A significant negative correlation was found between cumulative inbreeding depression and the primary selfing rate for the combined sample of angiosperms (N = 35) and gymnosperms (N = 9); the correlation was significant for angiosperms but not gymnosperms examined separately. The average inbreeding depression in predominantly selfing species (δ = 0.23) was significantly less (43%) than that in predominantly outcrossing species (δ = 0.53). These results support the theoretical prediction that selfing reduces the magnitude of inbreeding depression. Most self-fertilizing species expressed the majority of their inbreeding depression late in the life cycle, at the stage of growth/reproduction (14 of 18 species), whereas outcrossing species expressed much of their inbreeding depression either early, at seed production (17 of 40 species), or late (19 species). For species with four life stages examined, selfing and outcrossing species differed in the magnitude of inbreeding depression at the stage of seed production (selfing δ = 0.05, N = 11; outcrossing δ = 0.32, N = 31), germination (selfing δ = 0.02, outcrossing δ = 0.12), and survival to reproduction (selfing δ = 0.04, outcrossing δ = 0.15), but not at growth and reproduction (selfing δ = 0.21, outcrossing δ = 0.27); inbreeding depression in selfers relative to outcrossers increased from early to late life stages. These results support the hypothesis that most early acting inbreeding depression is due to recessive lethals and can be purged through inbreeding, whereas much of the late-acting inbreeding depression is due to weakly deleterious mutations and is very difficult to purge, even under extreme inbreeding.     

CORRELATED EVOLUTION OF MATING STRATEGY AND INBREEDING DEPRESSION WITHIN AND AMONG POPULATIONS OF THE HERMAPHRODITIC SNAIL PHYSA ACUTA

Inbreeding depression is one of the main forces opposing the evolution of self-fertilization. Of central importance is the hypothesis that inbreeding depression and selfing coevolve antagonistically, generating either low selfing rate and high inbreeding depression or vice versa. However, there is limited evidence for this coevolution within species. We investigated this topic in the hermaphroditic snail Physa acuta . In this species, isolated individuals delay the onset of egg laying compared to individuals having access to mates. Longer delays ("waiting times") indicate more intense selfing avoidance. We measured inbreeding depression and waiting time in a large quantitative-genetic experiment (281 outbred families derived from 26 natural populations). We observed large genetic variance for both traits and a strong positive genetic covariance between them, most of which resided within rather than among populations. It means that, within populations, individuals with higher mutation load avoided selfing more strongly on average. This genetic covariance may result from pleiotropy and/or linkage disequilibrium. Whatever its genetic architecture, the fact it emerges specifically when individuals are deprived of mates suggests it is not fortuitous and rather reflects the action of natural selection. We conclude that a diversity of mating strategies can arise within populations subjected to variation in inbreeding depression.     

THE ROLE OF INBREEDING DEPRESSION AND MATING SYSTEM IN THE EVOLUTION OF HETEROSTYLY

We investigated the role of morph‐based differences in the expression of inbreeding depression in loss of the mid‐styled morph from populations of tristylous Oxalis alpina. The extent of self‐compatibility (SC) of reproductive morphs, the degree of self‐fertilization, and the magnitude of inbreeding depression were investigated in three populations of O. alpina differing in their tristylous incompatibility relationships. All three populations exhibited significant inbreeding depression. In two populations with highly modified tristylous incompatibility, manifested as increased reciprocal compatibility between short‐ and long‐styled morphs, substantial SC and self‐fertilization of mid‐styled morphs were detected, and expected to result in expression of inbreeding depression in the progeny of mid‐styled morphs in the natural populations. In contrast, significant self‐fertility of the mid‐styled morph was absent from the population with typical tristylous incompatibility, and no self‐fertilization could be detected. Although self‐fertilization and expression of inbreeding depression should result in selection against the mid‐styled morph in the later stages of the transition from tristyly to distyly, in O. alpina selection against the mid‐styled morph in the early phases of the evolution of distyly is likely due to genic selection against mid‐alleles associated with modified tristylous incompatibility, rather than expression of inbreeding depression.     

LIFETIME ESTIMATES OF BIPARENTAL INBREEDING DEPRESSION IN THE SELF-INCOMPATIBLE ANNUAL PLANT RAPHANUS SATIVUS

Studies of inbreeding depression in plant populations have focused primarily on comparisons of selfing versus outcrossing in self-compatible species. Here we examine the effect of five naturally occurring levels of inbreeding (f ranging from 0 to 0.25 by pedigree) on components of lifetime fitness in a field population of the self-incompatible annual, Raphanus sativus. Pre- and postgermination survival and reproductive success were examined for offspring resulting from compatible cross-pollinations. Multiple linear regression of inbreeding level on rates of fruit and seed abortion as well as seed weight and total seed weight per fruit were not significant. Inbreeding level was not found to affect seed germination, offspring survival in the field, date of first flowering, or plant biomass (dry weight minus fruit). The effect of inbreeding on seedling viability in the greenhouse and viability to flowering was significant but small and inconsistently correlated with inbreeding level. Maternal fecundity, however, a measure of seed yield, was reduced almost 60% in offspring from full-sib crosses (f = 0.25) relative to offspring resulting from experimental outcross pollinations (f = 0). Water availability, a form of physiological stress, affected plant biomass but did not affect maternal fecundity, nor did it interact with inbreeding level to influence these characters. The delayed expression of strong inbreeding depression suggests that highly deleterious recessive alleles were not a primary cause of fitness loss with inbreeding. Highly deleterious recessives may have been purged by bottlenecks in population size associated with the introduction of Raphanus and its recent range expansions. In general, reductions in total relative fitness of greater than 50% associated with full-sib crosses should be sufficient to prohibit the evolution of self-compatibility via transmission advantage in Raphanus.     

THE RELATIONSHIP BETWEEN INBREEDING DEPRESSION AND PRIOR INBREEDING AMONG POPULATIONS OF FOUR MIMULUS TAXA

When recessive mutations are the primary cause of inbreeding depression, a negative relationship between the levels of prior inbreeding and inbreeding depression is expected. We tested this prediction using 15 populations chosen a priori to represent a wide range of prior inbreeding among four closely related taxa of the Mimulus guttatus species complex. Artificially selfed and outcrossed progeny were grown under controlled growth-chamber conditions, and inbreeding depression was estimated for each population as one minus the ratio of the fitness of selfed to outcrossed progeny. Estimates of inbreeding depression varied from 0% to 68% among populations. Inbreeding coefficients, estimated from electrophoretic assay of field-collected progenies, ranged from 0.02 to 0.76. All five fitness traits displayed a negative association between inbreeding depression and the inbreeding coefficient, but only height showed a statistically significant correlation. Inbreeding depression was also not correlated with the level of genetic variability. In addition, populations with similar levels of prior inbreeding showed significant differences of inbreeding depression, whereas populations with different levels of prior inbreeding showed similar inbreeding depression. Within populations, inbreeding depression did not differ between progeny selfed one versus two generations. Our results are weakly consistent with the recessive mutation model of inbreeding depression, but suggest that additional factors, including genotype-by-environment interaction and complex modes of inheritance, may influence the expression of inbreeding depression.     

FIVE GENERATIONS OF ENFORCED SELFING AND OUTCROSSING IN MIMULUS GUTTATUS: INBREEDING DEPRESSION VARIATION AT THE POPULATION AND FAMILY LEVEL

The focus of this study was to examine the consequences of five sequential generations of enforced selfing and outcrossing in two annual populations of the mixed-mating Mimulus guttatus. Our primary goal was to determine whether purging of deleterious recessive alleles occurs uniformly between populations and among families, and thus gain insights into the mode of gene action (dominance, overdominance, and/or epistasis) governing the expression of inbreeding depression at both the population and family levels across the life cycle.     

THE EFFECT OF INBREEDING IN DIPLOID AND TETRAPLOID POPULATIONS OF EPILOBIUM ANGUSTIFOLIUM (ONAGRACEAE): IMPLICATIONS FOR THE GENETIC BASIS OF INBREEDING DEPRESSION

The partial dominance model for the evolution of inbreeding depression predicts that tetraploids should exhibit less inbreeding depression than their diploid progenitors. We tested this prediction by comparing the magnitude of inbreeding depression in tetraploid and diploid populations of the herbaceous perennial Epilobium angustifolium (Onagraceae). Inbreeding depression was estimated in the greenhouse for three tetraploid and two diploid populations at four life stages. The mating system of a tetraploid population was estimated and compared to a previous estimate for diploids. Tetraploids showed less inbreeding depression than diploids at all life history stages, and these differences were significant for seed-set and cumulative fitness, but not for germination, survival, or plant dry mass at nine weeks. This result suggests that the genetic basis of inbreeding depression may differ among life stages. The primary selfing rate of the tetraploid population was r = 0.43, which is nearly identical to that of a diploid population (r = 0.45), indicating that differences in inbreeding depression between diploids and tetraploids are probably not due to differences in the mating system. Cumulative inbreeding depression, calculated from the four life history stages, was significantly higher for diploids () than for tetraploids (), supporting the partial dominance model of inbreeding depression.     

EVOLUTION OF BIPARENTAL CARE IN THE HERMAPHRODITIC POLYCHAETE WORM OPHRYOTROCHA DIADEMA

Ophryotrocha diadema is a simultaneously hermaphroditic polychaete worm with a brief adolescent protandrous phase. In the mating system of this worm, pairs are formed preferentially between simultaneous hermaphrodites. Both partners of a pair regularly alternate sex roles, reciprocate egg exchange, and care for developing embryos. It was experimentally shown that neglected eggs have a 31% probability of dying, but eggs cared for by both parents, by a single parent, or even by an unrelated individual have a 95% probability of developing. In pairs experimentally prevented from caring for eggs, intruders succeeded in substituting one of the partners significantly more frequently than in pairs allowed to care for eggs. Thus, the main adaptive value of biparental care would be to guarantee a partner for egg reciprocation. Protandrous males are inefficient brooders, and biparental care becomes fully established only when individuals are able to reciprocate egg exchange, i.e., they have reached the simultaneously hermaphroditic stage.     

THE EVOLUTION OF ASSORTATIVE MATING AND SELFING WITH IN- AND OUTBREEDING DEPRESSION

The effect of inbreeding and outbreeding depression on the evolution of assortment are often considered separately. For instance, inbreeding depression is usually thought to shape selfing rates whereas outbreeding depression is commonly thought to affect the evolution of assortative mating. In this article, we consider the evolution of assortment in a context of local adaptation and we show that it is a typical situation in which both effects act simultaneously to shape the degree of selfing or assortative mating. More specifically, we show that selection on a modifier of mating can be partitioned into three distinct effects: a transmission advantage, an association to heterozygosity (proportional to inbreeding depression), and an association to beneficial alleles (proportional to outbreeding depression), so that random mating may evolve even with strong local adaptation. In addition, we show that it is necessary to carefully delimit the conditions for polymorphism at local adaptation locus to study the evolution of assortment. In particular, the range of parameters most favorable to the maintenance of polymorphism corresponds to situations favoring less assortment.     

DISPERSAL AND PLANT MATING SYSTEMS: THE EVOLUTION OF SELF-FERTILIZATION IN SUBDIVIDED POPULATIONS

Intermediate rates of self-fertilization can be evolutionarily stable when the progeny of self-fertilization events are less successful migrants than those of outcrossing events, unless self-fertilization reduces an individual's contribution to the pollen pool by an amount equal to the rate at which it self-fertilizes. This result holds regardless of whether pollen or diaspores are more widely dispersed. The differential migration of selfed and outcrossed progeny may be a result of differential establishment with comparable rates of dispersal, or it may be a result of differential dispersal rates. In the first case, detailed predictions concerning the evolutionarily stable selfing rate can be made. In the second case, only qualitative predictions are possible in the absence of specific assumptions about how the migration rate is affected by the average selfing rate in each subpopulation.     

ESTIMATION OF PARAMETERS OF INBREEDING AND GENETIC DRIFT IN POPULATIONS WITH OVERLAPPING GENERATIONS

Many long‐lived plant and animal species have nondiscrete overlapping generations. Although numerous models have been developed to predict the effective sizes (N_e) of populations with overlapping generations, they are extremely difficult to apply to natural populations because of the large array of unknown and elusive life‐table parameters involved. Unfortunately, little work has been done to estimate the N_e of populations with overlapping generations from marker data, in sharp contrast to the situation of populations with discrete generations for which quite a few estimators are available. In this study, we propose an estimator (EPA, estimator by parentage assignments) of the current N_e of populations with overlapping generations, using the sex, age, and multilocus genotype information of a single sample of individuals taken at random from the population. Simulations show that EPA provides unbiased and accurate estimates of N_e under realistic sampling and genotyping effort. Additionally, it yields estimates of other interesting parameters such as generation interval, the variances and covariances of lifetime family size, effective number of breeders of each age class, and life‐table variables. Data from wild populations of baboons and hihi (stitchbird) were analyzed by EPA to demonstrate the use of the estimator in practical sampling and genotyping situations.     

THE EVOLUTION OF SELF-FERTILIZATION AND INBREEDING DEPRESSION IN PLANTS. II. EMPIRICAL OBSERVATIONS

A bimodal distribution of outcrossing rates was observed for natural plant populations, with more primarily selfing and primarily outcrossing species, and fewer species with intermediate outcrossing rate than expected by chance. We suggest that this distribution results from selection for the maintenance of outcrossing in historically large, outcrossing populations with substantial inbreeding depression, and from selection for selfing when increased inbreeding, due to pollinator failure or population bottlenecks, reduces the level of inbreeding depression. Few species or populations are fixed at complete selfing or complete outcrossing. A low level of selfing in primarily outcrossing species is unlikely to be selectively advantageous, but will not reduce inbreeding depression to the level where selfing is selectively favored, particularly if accompanied by reproductive compensation. Similarly, occasional outcrossing in primarily selfing species is unlikely to regularly provide sufficient heterosis to maintain selection for outcrossing through individual selection. Genetic, morphological and ecological constraints may limit the potential for outcrossing rates in selfers to be reduced below some minimum level.     

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.     

THE SIGNIFICANCE OF GENETIC EROSION IN THE PROCESS OF EXTINCTION. IV. INBREEDING DEPRESSION AND HETEROSIS EFFECTS CAUSED BY SELFING AND OUTCROSSING IN SCABIOSA COLUMBARIA

The effects of self-fertilization, within-population crosses (WPC) and between-population crosses (BPC) on progeny fitness were investigated in the greenhouse for Scabiosa columbaria populations of varying size. Plants grown from field collected seeds were hand pollinated to produce selfed, WPC, and BPC progeny. The performance of these progenies was examined throughout the entire life cycle. The different pollination treatments did not significantly affect germination, seedling-to-adult survival, flowering percentage and the number of flower heads. But severe inbreeding depression was demonstrated for biomass production, root development, adult survival, and seed set. Additionally, multiplicative fitness functions were calculated to compare relative fitnesses for progeny. On average, WPC progeny showed a more than 4-fold, and BPC progeny an almost 10-fold, advantage over selfed progeny, indicating that S. columbaria is highly susceptible to inbreeding. No clear relationship was found between population size and level of inbreeding depression, suggesting that the genetic load has not yet been reduced substantially in the small populations. A significant positive correlation was found between plant dry weight and total fitness. In two out of six populations, the differences between the effects of the pollination treatments on dry weight increased significantly when seedlings were grown under competitive conditions. This result is interpreted as an enhancement of inbreeding depression under these conditions. It is argued that improvement of the genetic exchange between populations may lower the probability of population extinction.