Levels of inbreeding depression over seven generations of selfing in the androdioecious clam shrimp, Eulimnadia texana

Androdioecy (mixtures of males and hermaphrodites) is a rare mating system in both plants and animals. Theory suggests that high levels of inbreeding depression can maintain males in androdioecious populations if hermaphrodites commonly self-fertilize. However, if inbreeding depression (delta) can be 'purged' from selfing populations, maintaining males is more difficult. In the androdioecious clam shrimp, Eulimnadia texana, delta is estimated to be as high as 0.7. Previous work suggests that this high level is maintained in the face of high levels of inbreeding due to an associative overdominance of fitness-related loci with the sex-determining locus. Such associative overdominance would make purging of inbreeding depression difficult to impossible. The current experiment was designed to determine if delta can be purged in these shrimp by tracking fitness across seven generations in selfing and outcrossing treatments. Evidence of purging was found in one of four populations, but the remaining populations demonstrated a consistent pattern of delta across generations. Although the experimental design allowed ample opportunity for purging, the majority of populations were unable to purge their genetic load. Therefore, delta in this species is likely due to associative overdominance caused by deleterious recessive alleles linked to the sex determining locus.     

INBREEDING DEPRESSION IN A SELF-COMPATIBLE,ANDRODIOECIOUS CRUSTACEAN,EULIMNADIA TEXANA

The observation that offspring produced by the mating of close relatives are often less fit than those produced by matings between unrelated individuals (i.e., inbreeding depression) has commonly been explained in terms of the increased probability of expressing deleterious recessive alleles among inbred offspring (the partial dominance model). This model predicts that inbreeding depression should be limited in regularly inbreeding populations because the deleterious alleles that cause inbreeding depression (i.e., the genetic load) should be purged by regularly exposing these alleles to natural selection. We indirectly test the partial dominance model using four highly inbred populations of an androdioecious crustacean, the clam shrimp Eulimnadia texana. These shrimp are comprised of males and hermaphrodites, the latter capable of either self-fertilizing or mating with a male (i.e., outcrossing between hermaphrodites is impossible). Hermaphrodites are further subdivided into monogenics (produced via self-fertilization) and amphigenics (produced via self-fertilization or outcrossing). Electrophoretic evidence suggests significant differences in heterozygosity among populations, but that selfing rates were not statistically different (average s = 0.67). Additional electrophoretic analyses reveal that three previously described sex-linked loci (Fum, Idh-1, and Idh-2) are all tightly linked to each other, with crossing over on the order of 1% per generation. Although selfing rates are clearly high, we present evidence that early inbreeding depression (hatching rates, juvenile survival, and age at sexual maturity) exists in all four populations. For all of these factors, inbreeding depression was inferred by the positive correlation of multilocus heterozygosity and fitness. Cumulative inbreeding depression (8) is between 0.41 and 0.47 across all populations, which appears to be too low to limit the effects of purging via identity disequilibrium. Instead, we suggest that the maintenance of inbreeding depression in these populations is due to the observed linkage group, which we suggest contains a large number of genes including many related to fitness. Segregation of such a large linkage group would explain our observations of the predominance of amphigenic hermaphrodites in our field samples and of survival differences between monogenics and amphigenics within selfed clutches. We propose that a modified form of the overdominance model for inbreeding depression operating at the level of linkage groups maintains the observed levels of inbreeding depression in these populations even in the face of high rates of selfing.     

Maternal sex and mate relatedness affect offspring quality in the gynodioecious Silene acaulis

In gynodioecious species, females sacrifice fitness by not producing pollen, and hence must have a fitness advantage over hermaphrodites. Because females are obligately outcrossed, they may derive a fitness advantage by avoiding selfing and inbreeding depression. However, both sexes are capable of biparental inbreeding, and there are currently few estimates of the independent effects of maternal sex and multiple levels of inbreeding on female advantage. To test these hypotheses, females and hermaphrodites from six Alaskan populations of Silene acaulis were crossed with pollen from self (hermaphrodites only), a sibling, a random plant within the same population, and a plant from a different population. Germination, survivorship and early growth revealed inbreeding depression for selfs and higher germination but reduced growth in sib-crosses, relative to outcrosses. Independent of mate relatedness, females germinated more seeds that grew faster than offspring from hermaphrodites. This indicates that inbreeding depression as well as maternal sex can influence breeding system evolution. The effect of maternal sex may be explained by higher performance of female genotypes and a greater abundance of female genotypes among the offspring of female mothers.     

INBREEDING DEPRESSION IN GYNODIOECIOUS LOBELIA SIPHILITICA: AMONG-FAMILY DIFFERENCES OVERRIDE BETWEEN-MORPH DIFFERENCES

If inbreeding depression is caused by deleterious recessive alleles, as suggested by the partial dominance hypothesis, a negative correlation between inbreeding and inbreeding depression is predicted. This hypothesis has been tested several times by comparisons of closely related species or comparisons of populations of the same species with different histories of inbreeding. However, if one is interested in whether this relationship contributes to mating-system evolution, which occurs within populations, comparisons among families within a population are needed; that is, inbreeding depression among individuals with genetically based differences in their rate of selfing should be compared. In gynodioecious species with self-compatible hermaphrodites, hermaphrodites will have a greater history of potential inbreeding via both selfing and biparental inbreeding as compared to females and may therefore express a lower level of inbreeding depression. We estimated the inbreeding depression of female and hermaphrodite lineages in gynodioecious Lobelia siphilitica in a greenhouse experiment by comparing the performance of selfed and outcrossed progeny, as well as sibling crosses and crosses among subpopulations. We did not find support for lower inbreeding depression in hermaphrodite lineages. Multiplicative inbreeding depression (based on seed germination, juvenile survival, survival to flowering, and flower production in the first growing season) was not significantly different between hermaphrodite lineages (δ = 0.30 ± 0.08) and female lineages (δ = 0.15 ± 0.18), although the trend was for higher inbreeding depression in the hermaphrodite lineages. The population-level estimate of inbreeding depression was relatively low for a gynodioecious species (δ = 0.25) and there was no significant inbreeding depression following biparental inbreeding (δ = 0.01). All measured traits showed significant variation among families, and there was a significant interaction between family and pollination treatment for four traits (germination date, date of first flowering, number of flowers, and aboveground biomass). Our results suggest that the families responded differently to selfing and outcrossing: Some families exhibited lower fitness following selfing whereas others seemed to benefit from selfing as compared to outcrossing. Our results support recent simulation results in that prior inbreeding of the lineages did not determine the level of inbreeding depression. These results also emphasize the importance of determining family-level estimates of inbreeding depression, relative to population-level estimates, for studies of mating-system evolution.     

Reproductive biology and relative male and female fitness in a trioecious cactus,Pachycereus pringlei (Cactaceae)

We describe the breeding system of an autotetraploid trioecious cactus, Pachycereus pringlei, provide estimates of the fitnesses of males and females relative to that of hermaphrodites, and discuss the role played by pollinators in the maintenance of three sexual morphs. Relatively high frequencies of females (45%) and males (26%) exist in coastal desert populations around Bahia Kino, Sonora, Mexico. They differ from hermaphrodites in flower size (females only), initiation of the flowering season, number of flowers produced per night and per season, sucrose content of nectar, and, in females, number of fruits produced per season under open pollination and in response to hand-pollination. Major similarities between the sex classes include overall plant size, nectar volume per flower, percent fruit set in open-pollinated flowers of females and hermaphrodites, seed mass and number of seeds per fruit, and pollen mass per flower in males and hermaphrodites. Hermaphrodites are self-compatible, and the selfing rate is high (65%). Levels of inbreeding depression in selfed fruits and seeds appear to be low. Fruit set is strongly pollinator-dependent in females but much less so in hermaphrodites. Relative fitness of males and females, as measured by annual production of pollen or seeds, is at least 1.5 times higher than that of the corresponding sex function in hermaphrodites. Given the high selfing rate and apparent lack of inbreeding depression, these fitness differences are insufficient to explain the occurrence of trioecy in this species.     

Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: do hermaphrodites need males for complete fertilization?

Androdioecy (populations comprised of mixtures of males and hermaphrodites) is a rare mating system, found only in a few plants and animals. The rarity of this system stems from the limited benefits to males in an otherwise all-hermaphroditic population. One of the potential benefits to males is typified by the nematode Caenorhabditis elegans, in which hermaphrodites do not produce sufficient sperm to fertilize all of their eggs. Here we explore the possibility that males are needed for complete fertilization of hermaphrodites' eggs in a second androdioecious animal, the clam shrimp Eulimnadia texana. We compare the fertilization rate of outcrossed to selfed eggs to test whether the latter exhibit lower fertilization due to sperm limitation (as in C. elegans). Because this comparison confounds differences in egg fertilization due to sperm limitation with the potential for early inbreeding depression, we also used a third mating treatment, a brother/sister cross, to allow separation of sperm limitation from inbreeding depression. In both populations examined, the proportion of eggs that were fertilized decreased linearly with increasing relatedness: comparing eggs produced by outcrossing, brother/sister, and selfed matings, respectively. This pattern suggests that differences in fertilization among these three treatments were caused solely by inbreeding depression, and therefore that hermaphrodites are not sperm limited. These results are combined with previous data on this species to test whether the maintenance of males can be explained using a population genetics model specifically designed for this species.     

Mating system contributes only slightly to female maintenance in gynodioecious Geranium maculatum (Geraniaceae)

Gynodioecy, the co-occurrence of female and hermaphroditic individuals within a population, is an important intermediate in the evolution of separate sexes. The first step, female maintenance, requires females to have higher seed fitness compared with hermaphrodites. A common mechanism thought to increase relative female fitness is inbreeding depression avoidance, the magnitude of which depends on hermaphroditic selfing rates and the strength of inbreeding depression. Less well studied is the effect of biparental inbreeding on female fitness. Biparental inbreeding can affect relative female fitness only if its consequence or frequency differs between sexes, which could occur if sex structure and genetic structure both occur within populations. To determine whether inbreeding avoidance and/or biparental inbreeding can account for female persistence in Geranium maculatum, we measured selfing and biparental inbreeding rates in four populations and the spatial genetic structure in six populations. Selfing rates of hermaphrodites were low and did not differ significantly from zero in any population, leading to females gaining at most a 1–14% increase in seed fitness from inbreeding avoidance. Additionally, although significant spatial genetic structure was found in all populations, biparental inbreeding rates were low and only differed between sexes in one population, thereby having little influence on female fitness. A review of the literature revealed few sexual differences in biparental inbreeding among other gynodioecious species. Our results show that mating system differences may not fully account for female maintenance in this species, suggesting other mechanisms may be involved.     

Consequences of inbreeding for offspring fitness and gender in Silene vulgaris,a gynodioecious plant

Abstract In gynodioecious plants, hermaphrodite and female plants co‐occur in the same population. In these systems gender typically depends on whether a maternally inherited cytoplasmic male sterility factor (CMS) is counteracted by nuclear restorer alleles. These restorer alleles are often genetically dominant. Although plants of the female morph are obligatorily outcrossing, hermaphrodites may self. This selfing increases homozygosity and may thus have two effects: (1) it may decrease fitness (i.e. result in inbreeding depression) and (ii) it may increase homozygosity of the nuclear restorer alleles and therefore increase the production of females. This, in turn, enhances outcrossing in the following generation. In order to test the latter hypothesis, experimental crosses were conducted using individuals derived from four natural populations of Silene vulgaris, a gynodioecious plant. Treatments included self‐fertilization of hermaphrodites, outcrossing of hermaphrodites and females using pollen derived from the same source population as the pollen recipients, and outcrossing hermaphrodites and females using pollen derived from different source populations. Offspring were scored for seed germination, survivorship to flowering and gender. The products of self‐fertilization had reduced survivorship at both life stages when compared with the offspring of outcrossed hermaphrodites or females. In one population the fitness of offspring produced by within‐population outcrossing of females was significantly less than the fitness of offspring produced by crossing females with hermaphrodites from other populations. Self‐fertilization of hermaphrodites produced a smaller proportion of hermaphroditic offspring than did outcrossing hermaphrodites. Outcrossing females within populations produced a smaller proportion of hermaphrodite offspring than did crossing females with hermaphrodites from other populations. These results are consistent with a cytonuclear system of sex determination with dominant nuclear restorers, and are discussed with regard to how the mating system and the genetics of sex determination interact to influence the evolution of inbreeding depression.     

MUTATIONAL MELTDOWN IN SELFING ARABIDOPSIS LYRATA

The majority of plant species and many animals are hermaphrodites, with individuals expressing both female and male function. Although hermaphrodites can potentially reproduce by self‐fertilization, they have a high prevalence of outcrossing. The genetic advantages of outcrossing are described by two hypotheses: avoidance of inbreeding depression because selfing leads to immediate expression of recessive deleterious mutations, and release from drift load because self‐fertilization leads to long‐term accumulation of deleterious mutations due to genetic drift and, eventually, to extinction. I tested both hypotheses by experimentally crossing Arabidopsis lyrata plants (self‐pollinated, cross‐pollinated within the population, or cross‐pollinated between populations) and measuring offspring performance over 3 years. There were 18 source populations, each of which was either predominantly outcrossing, mixed mating, or predominantly selfing. Contrary to predictions, outcrossing populations had low inbreeding depression, which equaled that of selfing populations, challenging the central role of inbreeding depression in mating system shifts. However, plants from selfing populations showed the greatest increase in fitness when crossed with plants from other populations, reflecting higher drift load. The results support the hypothesis that extinction by mutational meltdown is why selfing hermaphroditic taxa are rare, despite their frequent appearance over evolutionary time.     

Gender-specific inbreeding depression in a gynodioecious plant, Geranium maculatum (Geraniaceae)

In gynodioecious species, females coexist with hermaphrodites in natural populations even though hermaphrodites attract more pollinators, are capable of reproducing through pollen, and can self-fertilize. This study tests the hypothesis that inbreeding depression helps to maintain females in natural populations. It also examines whether gender lineages that differ in selfing rates might experience different levels of inbreeding depression. Female and hermaphroditic lineages of the gynodioecious species Geranium maculatum were used in self, sib-cross and outcross experiments to examine inbreeding depression levels and to determine whether these levels differ between hermaphroditic and female lineages. Six fitness correlates were measured in the greenhouse and compared among pollination types and between genders. Severe inbreeding depression was found for both individual fitness traits and cumulative fitness in early life history stages. Inbreeding depression levels were slightly higher in hermaphroditic than in female lineages, but this difference was not statistically significant. Because females are unable to self-pollinate and are less likely to experience inbreeding than hermaphrodites under natural conditions, these results suggest that severe inbreeding depression could confer a selective advantage for females that could help to maintain females in natural populations.     

Sex ratios and genetic variation in a functionally androdioecious species,Schizopepon bryoniaefolius (Cucurbitaceae)

Androdioecy, coexistence of hermaphrodites and males, is an extremely rare breeding system in angiosperms. In the present study, Schizopepon bryoniaefolius (Cucurbitaceae) was confirmed to be functionally androdioecious based on observations of floral and pollen morphology and bagging experiments. Six out of the 11 studied populations consisted of only hermaphrodites, while the other five populations were androdioecious and the frequencies of males were consistently lower than those of hermaphrodites (5.5–28.3%). To understand the consequences of an androdioecious breeding system, genetic variation was estimated using four polymorphic allozyme loci. The degree of genetic differentiation among 11 populations was high (G_ST = 0.688). Inbreeding coefficients (F_IS) for all loci significantly deviated from zero. In particular, the F_IS values averaged across the polymorphic loci in hermaphrodite populations were close to unity, suggesting that hermaphrodites are predominantly selfing in the absence of males. A significant negative correlation was found between the frequencies of males and inbreeding coefficients, indicating that outcrossing rates depend on the population sex ratio.     

ECOLOGICAL GENETICS OF GYNODIOECY IN SILENE VULGARIS: RELATIVE FITNESS OF FEMALES AND HERMAPHRODITES DURING THE COLONIZATION PROCESS

Recent theoretical models have addressed the influence of metapopulation dynamics on the fitness of females and hermaphrodites in gynodioecious plants. In particular, selection is thought to favor hermaphrodites during population establishment because that sex should be less prone to pollen limitation, especially if self-fertilization is possible. However, inbreeding depression could limit this advantage. In this experimental study of Silene vulgaris, a weedy gynodioecious plant, the fitness of females and hermaphrodites was estimated from seed production in both mixed-sex populations and for individuals isolated from these populations by 20, 40, 80, or 160 m. In mixed populations females display statistically significant greater per capita seed production owing to higher capsule production and higher rates of seed germination. The fitness of both sexes declines with increasing isolation, but at different rates, such that in the 160-m treatment hermaphrodites are by far the more fit sex. Allozyme studies suggest that this differential decline is because the selfing rate in hermaphrodites increases as a function of isolation, at least partially compensating for a decline in the availability of outcross pollen. Overall, the negative effects of pollen limitation on females far outweighs the negative effects of inbreeding depression following selfing in hermaphrodites. Thus, extinction/recolonization dynamics would appear to favor hermaphrodites as long as seed dispersal events exceed some critical distance.     

EVOLUTION OF UNISEXUALITY IN THE HAWAIIAN FLORA: A TEST OF MICROEVOLUTIONARY THEORY

The evolution of separate sexes as a means of avoiding self-fertilization requires the controversial coexistence of large inbreeding depression and high selfing rate in the ancestral hermaphrodite population. Fitness components of adult females and hermaphrodites in nature, of their open-pollinated progeny, and of experimental selfs and outcrosses onto hermaphrodites were compared in endemic Hawaiian Bidens sandvicensis, all of whose known populations are gynodioecious, consisting of a mixture of females and hermaphrodites. Multilocus selfing rates of hermaphrodites were also estimated, and sex morph ratio monitored over four seasons in three populations of B. sandvicensis and one population of gynodioecious B. cervicata. Total mean inbreeding depression in seed set (in the glasshouse), germination rate (in an open-air nursery on Kauai), and first year survivorship and fecundity in the field were estimated as 0.94 (SE 0.04), and occurred primarily in drought months. Lower survivorship and fecundity of selfs were partially explained by their consistently smaller size. Open-pollinated seed of females had significantly lower germination rate, proportion flowering, and fecundity than outcrossed progeny of hermaphrodites, suggesting moderate biparental inbreeding in females and a lack of any non-outcrossing advantage to progeny of females. In all fitness components, open-pollinated progeny of hermaphrodites were inferior to those of females and to outcrosses, and in most components were superior to selfs. Total performance of open-pollinated progeny of females relative to those of hermaphrodites was calculated as 2.3 (SE = 0.4), but since inflorescences of females also set 20% to 50% more seed than those of hermaphrodites, their total relative ovule success was estimated as 3.2 (SE = 0.5). If inheritance of male sterility is nuclear, this superiority is sufficient to maintain females in frequencies over 20% in populations, whose actual frequencies ranged from 14% to 33%. In four populations, selfing rates of hermaphrodites, assayed in seedlings, were 0.50, 0.45, 0.25, and 0.30, but since substantial inbreeding depression occurred prior to germination, the mean selfing rate of hermaphrodite ovules exceeded 0.57. Female frequencies were significantly higher in the two populations with higher hermaphrodite selfing rate. These results suggest that inbreeding depression can exert a profound influence on the mating system of self-compatible plants on Hawaii and perhaps other oceanic islands, and can be sufficiently strong to electively favor the elimination of the male function.     

EVOLUTION OF GYNODIOECY AND MAINTENANCE OF FEMALES: THE ROLE OF INBREEDING DEPRESSION,OUTCROSSING RATES,AND RESOURCE ALLOCATION IN SCHIEDEA ADAMANTIS (CARYOPHYLLACEAE)

Levels of inbreeding depression, outcrossing rates, and phenotypic patterns of resource allocation were studied to examine their relative importance in the maintenance of high numbers of females in gynodioecious Schiedea adamantis (Caryophyllaceae), an endemic Hawaiian shrub found in a single population on Diamond Head Crater, Oahu. In studies of inbreeding depression in two greenhouse environments, families of hermaphrodites exhibited significant inbreeding depression (δ = 0.60), based on a multiplicative fitness function using seeds per capsule, germination, survival, and the inflorescence biomass of progeny. Differences between inbred and outcrossed progeny were smallest at the early stage of seeds per capsule and more pronounced at the later stages of survival and inflorescence production. These results are consistent with inbreeding depression caused by many mutations of small effect. Using allozyme analyses, the inbreeding coefficient of adult plants in the field was not significantly different from zero, implying that δ in nature may be equal to one. The single locus estimate of the outcrossing rate for hermaphrodites was 0.50 based on progeny that survived to flowering; corrected for the disproportionate loss before flowering of progeny from selfing, the adjusted outcrossing rate at the zygote stage was 0.32, suggesting that considerable selfing occurs in hermaphrodites. Females were totally outcrossed. When females and hermaphrodites were compared for reproductive output in the field, females produced over twice as many seeds per plant as hermaphrodites, primarily because females had far more capsules per inflorescence than hermaphrodites. Females had greater mass per seed than hermaphrodites in the field, either because of greater provisioning or reduced inbreeding depression. There was no significant differential mortality with respect to sex over a seven year period. The higher number of seeds per plant of females, combined with substantial inbreeding depression and relatively high selfing rates for hermaphrodites, are probably responsible for the maintenance of females in this population. The predicted frequency of females based on data for seed production, the adjusted selfing rate, and inbreeding depression is 42%, remarkably close to the observed frequency of 39%. High levels of inbreeding depression suggest that considerable quantitative genetic variation is present for traits affecting fitness in this population, despite low allozyme variability and a presumed founder effect.     

INBREEDING DEPRESSION IN ANDRODIOECIOUS POPULATIONS OF DATISCA GLOMERATA (DATISCACEAE)

Several workers have suggested that the rarity of androdioecy (the presence of males and hermaphrodites in a breeding population) in nature is due to the large fitness gain required by male plants in order to be maintained by selection. As part of an ongoing investigation of this hypothesis, we tested the effects of selfing on fitness in functionally androdioecious populations of Datisca glomerata. We compared progeny from self-fertilizations, cross-fertilizations with pollen from male plants only, cross-fertilizations with pollen from hermaphrodite plants only, and open-pollinated flowers for several measures of progeny fitness including seed weight, germination rate, and seedling weight. Significant inbreeding depression was observed for androdioecious populations of D. glomerata for both seed and seedling weights. However, no significant differences were observed across treatments for seed germination percentages. The observation of significant levels of inbreeding depression in this study, combined with prior evidence of threefold greater pollen production by males, may at least partially account for the large fitness increase required by males to be maintained by selection.     

Do inbreeding depression and relative male fitness explain the maintenance of androdioecy in white mangrove, Laguncularia racemosa (Combretaceae)?

Mathematical models predict that to maintain androdioecious populations, males must have at least twice the fitness of male function in hermaphrodites. To understand how androdioecy is maintained in Laguncularia racemosa (white mangrove), outcrossing, inbreeding depression, and relative male fitness were estimated in two androdioecious populations and one hermaphroditic population. Outcrossing was estimated based on length of pollinator foraging bout and pollen carryover assumptions. Inbreeding depression was measured at three life stages: fruit set, seedling emergence, and seedling survivorship. The relative fitnesses of males and the male component of hermaphrodites were compared at these three stages and at the pollen production stage. Male frequency predictions generated by Lloyd's model were compared with observed frequencies in two androdioecious subpopulations. Outcrossing estimates were moderate for all populations (0.29-0.66). Inbreeding depression varied among populations (-0.03-0.86), but the strength of inbreeding depression did not increase with male frequency. Males produced significantly more flowers/inflorescence than hermaphrodites, but pollen production/flower did not differ. Male and hermaphroditic progeny did not differ significantly at other life stages. Populations of white mangrove with male plants were functionally androdioecious. Lloyd's model accurately predicted male frequency in one androdioecious subpopulation, but underestimated male frequency in the second subpopulation.     

Pollen limitation and the evolution of androdioecy from dioecy

Androdioecy is an unusual breeding system in which populations consist of separate male and hermaphrodite individuals. The evolution of androdioecy is still poorly understood; however, there is evidence from several androdioecious species that the breeding system may have evolved from dioecy (males and females). This article presents a simple deterministic model showing that androdioecy can evolve from dioecy under a broad range of realistic conditions. For the evolution of androdioecy from dioecy, hermaphrodites must be able to invade the dioecious population. Then, males must be maintained, while females are eliminated. Hermaphrodite invasion is favored when females are pollen limited and hermaphrodites have high overall fertility and are self-fertile. Male maintenance is favored when hermaphrodites resemble females, having high seed production and low pollen fitness, and when the selfing rate is not too high. These conditions were satisfied over a broad and realistic range of parameter values, suggesting that the evolution of androdioecy from dioecy is highly plausible.     

Inbreeding avoidance and the evolution of gender dimorphism in Wurmbea biglandulosa (Colchicaceae)

How females establish in populations of cosexuals is central to understanding the evolution of gender dimorphism in angiosperms. Inbreeding avoidance hypotheses propose that females can establish and be maintained if cosexual fitness is reduced because they self-fertilize, and their progeny express inbreeding depression. Here we assess the role of inbreeding avoidance in maintaining sexual system variation in Wurmbea biglandulosa. We estimated costs of self-pollination, mating patterns, and inbreeding depression in gender monomorphic (cosexuals only) and dimorphic (males and females) populations. Costs of selfing, estimated from seed set of experimentally self- and cross-pollinated flowers, were severe in both males and cosexuals (inbreeding depression, sigma = 0.86). In a field experiment, intact males that could self produced fewer seeds than both emasculated males and females, whereas seed set of intact and emasculated cosexuals did not differ. Thus, pollinator-mediated selfing reduces fitness of males but not cosexuals under natural conditions. Outcrossing rates of males revealed substantial selfing (t = 0.68), whereas females and cosexuals were outcrossed (0.92 and 0.97). For males, progeny inbreeding coefficients exceeded parental coefficients (0.220 vs. 0.009), whereas for females and cosexuals these coefficients did not differ and approached zero. Differences in coefficients between males and their progeny indicate that selfed progeny express severe inbreeding depression (sigma = 0.93). Combined with inbreeding depression for seed set, cumulative sigma = 0.99, indicating that most or all selfed zygotes fail to reach reproductive maturity. We propose that present sexual system variation in W. biglandulosa is maintained by high inbreeding depression coupled with differences in selfing rates among monomorphic and dimorphic populations.     

The inbreeding depression cost of selfing: Importance of flower size and population size in Collinsia parviflora (Veronicaceae)

Inbreeding depression should evolve with selfing rate when frequent inbreeding results in exposure of and selection against deleterious alleles. The selfing rate may be modified by plant traits such as flower size, or by population characteristics such as census size that can affect the probability of biparental inbreeding. Here we quantify inbreeding depression (δ) among different population sizes of Collinsia parviflora, a wildflower with interpopulation variation in flower size, by comparing fitness components and multiplicative fitness of experimentally produced selfed and outcrossed offspring. Selfed offspring had reduced multiplicative fitness compared to outcrossed offspring, but inbreeding depression was low in all combinations of population size and flower size (δ ≤ 0.05) except in large populations of large-flowered plants (δ = 0.45). The decrement to multiplicative fitness with inbreeding was not affected by population size nested within flower size, but differed between small- and large-flowered plants: small-flowered populations had lower overall inbreeding depression (δ = 0.04) compared to large-flowered populations (δ = 0.25). The difference in load with flower size suggests that either selection has removed deleterious recessive alleles or these alleles have become fixed in small-flowered, potentially more selfing populations, but that purging has not occurred to the same extent in presumably outcrossing large-flowered populations.     

HOW SELFING,INBREEDING DEPRESSION,AND POLLEN LIMITATION IMPACT NUCLEAR‐CYTOPLASMIC GYNODIOECY: A MODEL

Gynodioecy, the co‐occurrence of females and hermaphrodites, is often due to conflicting interactions between cytoplasmic male sterility genes and nuclear restorers. Although gynodioecy often occurs in self‐compatible species, the effect of self‐pollination, inbreeding depression, and pollen limitation acting differently on females and hermaphrodites remains poorly known in the case of nuclear‐cytoplasmic gynodioecy (NCG). In this study, we model NCG in an infinite population and we study the effect of selfing rate, inbreeding depression, and pollen limitation on the maintenance of gynodioecy and on sex ratios at equilibrium. We found that selfing and inbreeding depression have a strong impact, which depends on whether restorer cost acts on male or female fitness. When cost affects male fitness, the strength of cost has no effect, whereas selfing and inbreeding depression only impact gynodioecy by modifying the value of the female advantage. When cost affects female fitness, selfing facilitates NCG and reduces the role of strength of the cost, even when no inbreeding depression occurs, whereas inbreeding depression globally restricts the maintenance of the polymorphism. Finally, we found that pollen limitation could additionally strongly modify the dynamic of gynodioecy. We discuss our findings in the light of empirical data available in gynodioecious species.