Little to no inbreeding depression in a tapeworm with mixed mating

Meta‐studies on hermaphrodites have found a negative relationship between primary selfing rates and levels of inbreeding depression (ID) and, thus, generally support purging in inbred systems. However, in plants, high among‐taxa variance in ID results in no difference in the mean ID between outcrossing and mixed‐mating taxa. Selective interference likely explains high ID among mixed‐mating taxa, whereas low levels of ID among mixed‐mating taxa are not as stressed. Among animal hermaphrodites, primarily molluscs, there are little data on mixed‐mating systems. To fill a taxonomic and mating system gap, we tested for ID in a mixed‐mating tapeworm, Oochoristica javaensis. We provide a direct estimate of ID across infection of an intermediate host by comparing selfing rates at two life history stages. We found little to no evidence for ID, and the level of ID falls in line with what is reported for highly selfing species even though O. javaensis has mixed mating. We discuss this result within the context of kin mating in O. javaensis. Our results emphasize that primary selfing rates alone may be insufficient to classify the inbreeding history in all species when testing for a relationship to ID. Mixed‐mating taxa, and possibly some outcrossing taxa, may exhibit low levels of ID if biparental inbreeding is also driving purging. We advocate that ID studies report estimates of inbreeding history (e.g. F_IS or identity disequilibrium) from nature‐derived adult samples to provide context rather than relying on primary selfing rates alone.     

Occurrence,costs and heritability of delayed selfing in a free‐living flatworm

Evolutionary theory predicts that in the absence of outcrossing opportunities, simultaneously hermaphroditic organisms should eventually switch to self‐fertilization as a form of reproductive assurance. Here, we report the existence of facultative self‐fertilization in the free‐living flatworm Macrostomum hystrix, a species in which outcrossing occurs via hypodermic insemination of sperm into the parenchyma of the mating partner. First, we show that isolated individuals significantly delay the onset of reproduction compared with individuals with outcrossing opportunities (‘delayed selfing’) as predicted by theory. Second, consistent with the idea of M. hystrix being a preferential outcrosser under natural conditions, we report likely costs of selfing manifested via reduced hatchling production and offspring survival. Third, we demonstrate that selfing propensity has a genetic basis in this species, with a heritability estimated at 0.43 ± 0.11. Variation in selfing propensity could arise due to differing costs of inbreeding among families; despite marked inter‐family variation in apparent costs of inbreeding, we found no evidence for such a link. Alternatively, selfing propensity might differ across families because of heritable variation in reproductive traits that determine the likelihood of selfing. We speculate that adaptations to hypodermic insemination under outcrossing, most notably a highly modified copulatory stylet (male copulatory organ) and reduced sperm complexity, could also facilitate facultative selfing in this species.     

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.     

Experimental and genetic analyses reveal that inbreeding depression declines with increased self‐fertilization among populations of a coastal dune plant

Theory predicts that inbreeding depression (ID) should decline via purging in self‐fertilizing populations. Yet, intraspecific comparisons between selfing and outcrossing populations are few and provide only mixed support for this key evolutionary process. We estimated ID for large‐flowered (LF), predominantly outcrossing vs. small‐flowered (SF), predominantly selfing populations of the dune endemic Camissoniopsis cheiranthifolia by comparing selfed and crossed progeny in glasshouse environments differing in soil moisture, and by comparing allozyme‐based estimates of the proportion of seeds selfed and inbreeding coefficient of mature plants. Based on lifetime measures of dry mass and flower production, ID was stronger in nine LF populations [mean δ = 1?(fitness of selfed seed/fitness of outcrossed seed) = 0.39] than 16 SF populations (mean δ = 0.03). However, predispersal ID during seed maturation was not stronger for LF populations, and ID was not more pronounced under simulated drought, a pervasive stress in sand dune habitat. Genetic estimates of δ were also higher for four LF (δ = 1.23) than five SF (δ = 0.66) populations; however, broad confidence intervals around these estimates overlapped. These results are consistent with purging, but selective interference among loci may be required to maintain strong ID in partially selfing LF populations, and trade‐offs between selfed and outcrossed fitness are likely required to maintain outcrossing in SF populations.     

Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.     

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.     

LIFETIME INBREEDING DEPRESSION,PURGING, AND MATING SYSTEM EVOLUTION IN A SIMULTANEOUS HERMAPHRODITE TAPEWORM

Classical theory on mating system evolution suggests that simultaneous hermaphrodites should either outcross if they have high inbreeding depression (ID) or self‐fertilize if they have low ID. However, a mixture of selfing and outcrossing persists in many species. Previous studies with the tapeworm Schistocephalus solidus have found worms to self‐fertilize some of their eggs despite ID. The probability for selfing to spread depends on the relative fitness of selfers, as well as the genetic basis for ID and whether it can be effectively purged. We bred S. solidus through two consecutive generations of selfing and recorded several fitness correlates over the whole life cycle. After one round of selfing, ID was pronounced, particularly in early‐life traits, and the conservatively estimated lifetime fitness of selfed progeny was only 9% that of the outcrossed controls. After a second generation of selfing, ID remained high but was significantly reduced in several traits, which is consistent with the purging of deleterious recessive alleles (the estimated load of lethal equivalents dropped by 48%). Severe ID, even if it can be rapidly purged, likely prevents transitions toward pure selfing in this parasite, although we also cannot exclude the possibility that low‐level selfing has undetected benefits.     

Inbreeding depression and selfing rates in a self-compatible,hermaphroditic species,Schiedea membranacea (Caryophyllaceae)

Inbreeding depression and selfing rates were investigated in Schiedea membranacea (Caryophyllaceae), a hermaphroditic species endemic to the Hawaiian Islands. Most theoretical models predict high inbreeding depression in outcrossing hermaphroditic species and low inbreeding depression in inbreeding species. Although high outcrossing rates and high levels of inbreeding depression are characteristic of many species of Schiedea, self- fertilization is common among relatives of hermaphroditic S. membranacea, and high selfing rates and low levels of inbreeding depression were predicted in this species. Sixteen individuals grown in the greenhouse were used to produce selfed and outcrossed progeny. Inbreeding depression, which was evident throughout the stages measured (percentage viable seeds per capsule, mean seed mass, percentage seed germination, percentage seedling survival, and biomass after 8 mo), averaged 0.70. Inbreeding depression among maternal families varied significantly for all measured traits and ranged from −0.12 to 0.97. Using isozyme analysis, the multilocus selfing rate varied from 0.13 to 0.38 over 4 yr. Contrary to the initial prediction of high selfing and low inbreeding depression based on phylogenetic relationships within Schiedea, low selfing rates and high levels of inbreeding depression were found in S. membranacea. These results indicate that outcrossing is stable in this species and maintained by high levels of 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.     

Relatively weak inbreeding depression in selfing but also in outcrossing populations of North American Arabidopsis lyrata

Hermaphroditic plants can potentially self‐fertilize, but most possess adaptations that promote outcrossing. However, evolutionary transitions to higher selfing rates are frequent. Selfing comes with a transmission advantage over outcrossing, but self‐progeny may suffer from inbreeding depression, which forms the main barrier to the evolution of higher selfing rates. Here, we assessed inbreeding depression in the North American herb Arabidopsis lyrata, which is normally self‐incompatible, with a low frequency of self‐compatible plants. However, a few populations have become fixed for self‐compatibility and have high selfing rates. Under greenhouse conditions, we estimated mean inbreeding depression per seed (based on cumulative vegetative performance calculated as the product of germination, survival and aboveground biomass) to be 0.34 for six outcrossing populations, and 0.26 for five selfing populations. Exposing plants to drought and inducing defences with jasmonic acid did not magnify these estimates. For outcrossing populations, however, inbreeding depression per seed may underestimate true levels of inbreeding depression, because self‐incompatible plants showed strong reductions in seed set after (enforced) selfing. Inbreeding‐depression estimates incorporating seed set averaged 0.63 for outcrossing populations (compared to 0.30 for selfing populations). However, this is likely an overestimate because exposing plants to 5% CO₂ to circumvent self‐incompatibility to produce selfed seed might leave residual effects of self‐incompatibility that contribute to reduced seed set. Nevertheless, our estimates of inbreeding depression were clearly lower than previous estimates based on the same performance traits in outcrossing European populations of A. lyrata, which may help explain why selfing could evolve in North American A. lyrata.     

STRONG INBREEDING DEPRESSION IN TWO SCANDINAVIAN POPULATIONS OF THE SELF‐INCOMPATIBLE PERENNIAL HERB ARABIDOPSIS LYRATA

Inbreeding depression is a key factor influencing mating system evolution in plants, but current understanding of its relationship with selfing rate is limited by a sampling bias with few estimates for self‐incompatible species. We quantified inbreeding depression (δ) over two growing seasons in two populations of the self‐incompatible perennial herb Arabidopsis lyrata ssp. petraea in Scandinavia. Inbreeding depression was strong and of similar magnitude in both populations. Inbreeding depression for overall fitness across two seasons (the product of number of seeds, offspring viability, and offspring biomass) was 81% and 78% in the two populations. Chlorophyll deficiency accounted for 81% of seedling mortality in the selfing treatment, and was not observed among offspring resulting from outcrossing. The strong reduction in both early viability and late quantitative traits suggests that inbreeding depression is due to deleterious alleles of both large and small effect, and that both populations experience strong selection against the loss of self‐incompatibility. A review of available estimates suggested that inbreeding depression tends to be stronger in self‐incompatible than in self‐compatible highly outcrossing species, implying that undersampling of self‐incompatible taxa may bias estimates of the relationship between mating system and inbreeding depression.     

Mating system variation along a successional gradient in the allogamous and colonizing plant Crepis sancta (Asteraceae)

We analysed mating system in an annual and colonizing plant, Crepis sancta, that occupies different successional stages in the French Mediterranean region. Based on a previous experiment, we hypothesized that low inbreeding depression measured in young successional stages should select for selfing whereas higher inbreeding depression in old stages should select for outcrossing. Nine populations of C. sancta (Asteraceae) from contrasting successional stages were used to analyse (1) Seed set after autonomous and enforced selfing in controlled conditions and (2) outcrossing rates in natural conditions using allozymes (progeny array analysis). We found that C. sancta possesses a pseudo‐self‐incompatibility system and that mating system varies among populations. Allozymes revealed that the population multilocus outcrossing rates vary from 0.77 to 0.99. The lowest outcrossing rates occur in the youngest successional stages and complete outcrossing is found in old stages. The data partially agree with the predictions we made and the results are more generally discussed in the light of factors changing during succession. We did not find any evidence of reproductive assurance in the nine populations, contrary to what is often assumed as a major factor governing mating system evolution in colonizing species. We propose that mating system variation can be interpreted as the result of the balance between the cost of outcrossing and inbreeding depression in a metapopulation context.     

OUTCROSSING RATE AND INBREEDING DEPRESSION IN TWO ANNUAL MONOECIOUS HERBS,BEGONIA HIRSUTA AND B. SEMIOVATA

Most models of mating-system evolution predict inbreeding depression to be low in inbred populations due to the purging of deleterious recessive alleles. This paper presents estimates of outcrossing rates and inbreeding depression for two highly selfing, monoecious annuals Begonia hirsuta and B. semiovata. Outcrossing rates were estimated using isozyme polymorphisms, and the magnitude of inbreeding depression was quantified by growing progeny in the greenhouse produced through controlled selfing and outcrossing. The estimated single-locus outcrossing rate was 0.03 ± 0.01 (SE) for B. hirsuta and 0.05 ± 0.02 for B. semiovata. In both species, the seed production of selfed flowers was on average 12% lower than that of outcrossed flowers (B. hirsuta P = 0.07, B. semiovata P < 0.05, mixed model ANOVAs). There was no significant effect of crosstype on germination rate or survival, but selfed offspring had a lower dry mass than outcrossed offspring 18 weeks after planting in both species (on average 18% lower in B. hirsuta and 31% lower in B. semiovata). Plants that were the products of selfing began flowering later than plants produced through outcrossing in B. semiovata, but not in B. hirsuta. The effects of crosstype on seed production (B. semiovata), days to first flower and offspring dry mass (both species) varied among maternal parents, as indicated by significant crosstype x maternal parent interactions for these characters. Both species showed significant inbreeding depression for total fitness (estimated as the product of seed production, germination rate, survival and dry mass at 18 weeks). In B. hirsuta, the average total inbreeding depression was 22% (range -57%-98%; N = 23 maternal parents), and in B. semiovata, it was 42% (-11%-84%; N = 21). This study demonstrates that highly selfing populations can harbor substantial inbreeding depression. Our findings are consistent with the hypothesis that a high mutation rate to mildly deleterious alleles contributes to the maintenance of inbreeding depression in selfing populations.     

RECONSTRUCTING ORIGINS OF LOSS OF SELF‐INCOMPATIBILITY AND SELFING IN NORTH AMERICAN ARABIDOPSIS LYRATA: A POPULATION GENETIC CONTEXT

Theoretical and empirical comparisons of molecular diversity in selfing and outcrossing plants have primarily focused on long‐term consequences of differences in mating system (between species). However, improving our understanding of the causes of mating system evolution requires ecological and genetic studies of the early stages of mating system transition. Here, we examine nuclear and chloroplast DNA sequences and microsatellite variation in a large sample of populations of Arabidopsis lyrata from the Great Lakes region of Eastern North American that show intra‐ and interpopulation variation in the degree of self‐incompatibility and realized outcrossing rates. Populations show strong geographic clustering irrespective of mating system, suggesting that selfing either evolved multiple times or has spread to multiple genetic backgrounds. Diversity is reduced in selfing populations, but not to the extent of the severe loss of variation expected if selfing evolved due to selection for reproductive assurance in connection with strong founder events. The spread of self‐compatibility in this region may have been favored as colonization bottlenecks following glaciation or migration from Europe reduced standing levels of inbreeding depression. However, our results do not suggest a single transition to selfing in this system, as has been suggested for some other species in the Brassicaceae.     

Different levels of inbreeding depression between outcrossing and selfing Serapias species

We quantified inbreeding depression for fruit production, embryo vitality and seed germination in three deceptive orchids, Serapias vomeracea, S. cordigera and S. parviflora, which do not provide any reward to their pollinators, and are predicted to experience high outcrossing. Of the three species examined only S. parviflora was autonomously selfing. Both S. vomeracea and S. cordigera showed highly significant differences in fitness between selfed and outcrossed progenies, resulting in high levels of inbreeding depression, which increased in magnitude from seed set to seed germination. Inbreeding depression may promote outcrossing in Serapias by acting as a post-pollination barrier to selfing. Cumulative inbreeding depression across three stages in S. parviflora was lower that in both outcrossing species. The large difference in germination between selfed and outcrossed seeds is an important issue in conservation biology.     

Gynostemium micromorphology and pollination in Epipactis microphylla (Orchidaceae)

Self-pollination conditions have been recorded frequently in local populations of the genus Epipactis, and structural modifications have sometimes been reported, supporting taxonomic recognition of new species. As part of a survey of gynostemium micromorphology of Italian Epipactis populations, we studied an Apennine population of Epipactis microphylla (Ehrh.) Sw. a species listed as autogamous but with residual allogamous characters. In this population we observed the tendency to perform pre-anthesis cleistogamy. However, self-pollination was not a consequence of modification in column morphology. Cryptic pollen germination occurred in anther thecae or in the clinandrium, bypassing any contact with the receptive stigma. Pollen germination started from the distal pool of the pollinium, close to the rostellum-viscidium, suggesting that the rostellum-viscidium may have a function in promoting pollen-tube growth. Germinated pollen was exposed at the anthesis.     

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.     

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.     

Costs of selfing prevent the spread of a self‐compatibility mutation that causes reproductive assurance

In flowering plants, shifts from outcrossing to partial or complete self‐fertilization have occurred independently thousands of times, yet the underlying adaptive processes are difficult to discern. Selfing's ability to provide reproductive assurance when pollination is uncertain is an oft‐cited ecological explanation for its evolution, but this benefit may be outweighed by costs diminishing its selective advantage over outcrossing. We directly studied the fitness effects of a self‐compatibility mutation that was backcrossed into a self‐incompatible (SI) population of Leavenworthia alabamica, illuminating the direction and magnitude of selection on the mating‐system modifier. In array experiments conducted in two years, self‐compatible (SC) plants produced 17–26% more seed, but this advantage was counteracted by extensive seed discounting—the replacement of high‐quality outcrossed seeds by selfed seeds. Using a simple model and simulations, we demonstrate that SC mutations with these attributes rarely spread to high frequency in natural populations, unless inbreeding depression falls below a threshold value (0.57 ≤ δ_threshold ≤ 0.70) in SI populations. A combination of heavy seed discounting and inbreeding depression likely explains why outcrossing adaptations such as self‐incompatibility are maintained generally, despite persistent input of selfing mutations, and frequent limits on outcross seed production in nature.     

FLORAL CORRELATES AND FITNESS CONSEQUENCES OF MATING-SYSTEM VARIATION IN TURNERA ULMIFOLIA

Outcrossing rates varied from 0% to 69% among Jamaican populations of Turnera ulmifolia. A correlation between increasing herkogamy and outcrossing rate occurred among populations. Predictions from sex-allocation theory were tested by estimating allocation to reproductive functions. Significant differences in allocation patterns occurred among populations, but they were not correlated with outcrossing rates. The fitness consequences of inbreeding were assessed in high- and low-density greenhouse experiments for nine populations with variable outcrossing rates. No evidence for inbreeding depression occurred in early portions of the life history, but multiplicative fitness functions provide evidence for inbreeding depression. We tested the prediction that selfing populations have lower levels of inbreeding depression than outcrossing populations but found no significant correlation.