MIXED MATING SYSTEMS IN HAWAIIAN BIDENS (ASTERACEAE)

Floral features related to the breeding system were studied for 11 species of Hawaiian Bidens. Protandry and male sterility promote outcrossing, while self-compatibility and geitonogamy contribute to inbreeding. The combination of these floral mechanisms results in a mixed mating system in all species studied. Outcrossing rates of 15 populations of these species ranged from 0.43 to 0.88, averaging 0.65. Apparent selling rates of females ranged from 0 to 0.25 in seven gynodioecious populations surveyed, suggesting that there is variation in the level of biparental inbreeding among populations. The presence of females increased the level of outcrossing by an average of 9% in gynodioecious populations. This study indicates that the efficiency of gynodioecy as an outcrossing mechanism largely depends on the current outcrossing rate of hermaphrodites, the frequency of females, and the extent of genetic substructuring in populations. On average, autogamy contributed 4%, geitonogamy contributed 24%, and consanguineous mating contributed 15% to the realized selfing rate (43%) in the hermaphrodites of these species.     

Breeding systems of hermaphroditic and gynodioecious populations of the colonizing species Trifolium hirtum All. in California

Summary A multilocus procedure was used to estimate outcrossing rates in ten roadside populations of Trifolium hirtum in California. Three groups of populations were studied: cultivars, hermaphroditic, and gynodioecious (sexually dimorphic) populations. The multilocus outcrossing rate (t_m) varied from 0.05 to 0.43 among populations. Population level t_m estimates were significantly correlated with the observed heterozygosity in gynodioecious populations but not in hermaphroditic populations. The outcrossing rate of hermaphrodites and females was estimated in three gynodioecious populations; the estimates of t_m varied from 0.09 to 0.23 for hermaphrodites and from 0.73 to 0.80 for females. The distribution of outcrossing rates in gynodioecious populations is bimodal. Our results indicate that for the levels of selfing observed among hermaphrodites, inbreeding depression is likely to be a major factor in the maintenance of females in gynodioecious populations.     

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.     

Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success

 In gynodioecious species, females contribute genes to future generations only through ovules, and to persist in populations they must have a compensatory advantage compared with hermaphrodites that reproduce via ovules and pollen. This compensation can result from greater fecundity and/or superior success of progeny from females. We examined differences in seed production and progeny success between females and hermaphrodites in the geophyte Wurmbea biglandulosa to explain the maintenance of females. Females produced more ovuliferous flowers and had more ovules per flower than did hermaphrodites but this did not necessarily result in greater fecundity, in part because seed production of females was pollen-limited. Over four years in one population, open-pollinated females produced 1.32 more seeds than open-pollinated hermaphrodites (range 1.09–1.63). In two other populations examined for one year only females produced 1.07 and 0.79 as many seeds as hermaphrodites. Seed production of open-pollinated females and hermaphrodites was only 55% and 73% that of cross-pollinated plants, respectively, indicating that both genders were pollen-limited but females more so than hermaphrodites. Open-pollinated seeds from females were 1.18–1.27 times more likely to germinate than seeds from hermaphrodites. No gender differences existed in seedling growth or survival. Hermaphrodites were self-compatible, but selfed seed set was only 80% that of crossed seed set. Crossed seed set of females and hermaphrodites did not differ. Assuming nuclear control of male sterility, relative female fitness is insufficient to maintain females at their current frequencies of 17%, and substantial female fitness advantages at later life-cycle stages are required. Received May 4, 2001 Accepted February 25, 2002     

The functional ecology of gynodioecy in Eritrichum aretioides (Boraginaceae), the alpine forget-me-not

Eritrichum aretioides is a gynodioecious species with female and hermaphrodite individuals. In populations on Pennsylvania Mountain in central Colorado (USA), the frequency of females ranges from 22 to 41%. Flower number and the number of seeds produced per flower were similar in hermaphrodites and females. However, hermaphrodites produced larger flowers, while females produced larger seeds (P < 0.05 for both). In the field, seed germination was higher for seeds from females than for seeds from hermaphrodites (20 vs. 9% germination; P < 0.05). Unvisited flowers and open-pollinated flowers of hermaphrodites had similar pollen receipt (approx 20 pollen grains per stigma), but seed set following autogamous pollination was significantly lower than seed set following natural pollination. This finding indicates that hermaphrodites have a barrier to selfing and implies that the larger seed size and greater establishment advantage of offspring from females is unlikely to have resulted from female outcrossing advantage. Rather, differences in the quality of seed progeny between morphs probably reflect a trade-off in sexual allocation or pleiotropic effects of the sex-determining genes.     

Mating system, sex ratio, and persistence of females in the gynodioecious shrub Daphne laureola L. (Thymelaeaceae)

Although in gynodioecious populations male steriles require a fecundity advantage to compensate for their gametic disadvantage, southern Spanish populations of the long-lived shrub Daphne laureola do not show any fecundity advantage over hermaphrodites in terms of seed production and early seedling establishment. By using allozyme markers, we assess the mating system of this species in five populations differing in sex ratio, and infer levels of inbreeding depression over the whole life cycle by comparing the inbreeding coefficients at the seed and adult plant stages. Extremely low outcrossing rates (0.001相似文献   

Evidence of gynodioecy and sex ratio variation in Wurmbea biglandulosa (Colchicaceae)

 A valuable approach to understanding the evolution of gender dimorphism involves studies of single species that exhibit intraspecific variation in sexual systems. Here we survey sex ratios in 35 populations of Wurmbea biglandulosa, previously described as hermaphroditic. We found pronounced intraspecific variation in sexual systems; populations in the northeastern part of the species' range were hermaphroditic, whereas other populations were gynodioecious and contained 2–44% females. Populations with lower annual rainfall were more likely to be gynodioecious, supporting the view that gender dimorphism evolves more frequently in harsher environments. In gynodioecious populations, however, female frequency was not related to either annual rainfall or habitat, indicating that other factors are important in determining sex ratio variation. Females had smaller flowers and shorter stems than did hermaphrodites, potentially providing a basis for resource compensation. A female fecundity advantage may contribute to the maintenance of females in populations because females produced more ovuliferous flowers and had more ovules per flower than did hermaphrodites. Received March 2, 2001 Accepted February 25, 2002     

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.     

FREQUENCY-DEPENDENT FITNESS IN SILENE VULGARIS,A GYNODIOECIOUS PLANT

In gynodioecious plants the selective processes that determine the relative number of female and hermaphroditic individuals are often frequency dependent. Frequency-dependent fitness can occur in the two sexes through a variety of mechanisms, especially given pollen limitation and inbreeding depression when hermaphrodites are rare. Frequency dependence in several components of the fitness of female and hermaphroditic Silene vulgaris was tested in experiments in which the relative numbers of the two sexes was varied among 12 artificial populations. In females, the proportion of flowers that set fruit covaried positively among populations with the frequency of hermaphrodites in two separate experiments, whereas the number of flowers/plant covaried negatively in one case. In hermaphrodites, the number of seeds/fruit covaried positively with the frequency of hermaphrodites, whereas the fitness of hermaphrodites estimated through pollen transfer covaried negatively. The results are discussed as they relate to the selective maintenance of gynodioecy in S. vulgaris and in light of a recent model of the effect of population structure on selection in gynodioecious systems.     

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.     

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.     

Inbreeding effects on progeny sex ratio and gender variation in the gynodioecious Silene vulgaris (Caryophyllaceae)

In gynodioecious species, sex expression is generally determined through cytoplasmic male sterility genes interacting with nuclear restorers of the male function. With dominant restorers, there may be an excess of females in the progeny of self-fertilized compared with cross-fertilized hermaphrodites. Moreover, the effect of inbreeding on late stages of the life cycle remains poorly explored. Here, we used hermaphrodites of the gynodioecious Silene vulgaris originating from three populations located in different valleys in the Alps to investigate the effects of two generations of self- and cross-fertilization on sex ratio and gender variation. We detected an increase in females in the progeny of selfed compared with outcrossed hermaphrodites and inbreeding depression for female and male fertility. Male fertility correlated positively with sex ratio differences between outbred and inbred progeny, suggesting that dominant restorers are likely to influence male fertility qualitatively and quantitatively in S. vulgaris. We argue that the excess of females in the progeny of selfed compared with outcrossed hermaphrodites and inbreeding depression for gamete production may contribute to the maintenance of females in gynodioecious populations of S. vulgaris because purging of the genetic load is less likely to occur.     

Floral dimorphism, pollination, and self-fertilization in gynodioecious GERANIUM RICHARDSONII (Geraniaceae)

The selective maintenance of gynodioecy depends on the relative fitness of the male-sterile (female) and hermaphroditic morphs. Females may compensate for their loss of male fitness by reallocating resources from male function (pollen production and pollinator attraction) to female function (seeds and fruits), thus increasing seed production. Females may also benefit from their inability to self-fertilize if selfing and inbreeding depression reduce seed quality in hermaphrodites. We investigated how differences in floral resource allocation (flower size) between female and hermaphroditic plants affect two measures of female reproductive success, pollinator visitation and pollen receipt, in gynodioecious populations of Geranium richardsonii in Colorado. Using emasculation treatments in natural populations, we further examined whether selfing by autogamy and geitonogamy comprises a significant proportion of pollen receipt by hermaphrodites. Flowers of female plants are significantly smaller than those of hermaphrodites. The reduction in allocation to pollinator-attracting structures (petals) is correlated with a significant reduction in pollinator visitation to female flowers in artificial arrays. The reduction in attractiveness is further manifested in significantly less pollen being deposited on the stigmas of female flowers in natural populations. Autogamy is rare in these protandrous flowers, and geitonogamy accounts for most of the difference in pollen receipt between hermaphrodites and females. Female success at receiving pollen was negatively frequency dependent on the relative frequency of females in populations. Thus, two of the prerequisites for the maintenance of females in gynodioecious populations, differences in resource allocation between floral morphs and high selfing rates in hermaphrodites, occur in G. richardsonii.     

AN ECOLOGICAL GENETIC STUDY OF GYNODIOECY IN LIMNANTHES DOUGLASII (LIMNANTHACEAE)

Gynodioecy in two populations of Limnanthes douglasii var. rosea was studied for its maintenance requirements, role in population structure and its influence on the levels of outbreeding. The mode of inheritance of male sterility appeared to be nucleo-cytoplasmic, although the precise number of nuclear genes and dominance relationships could not be ascertained. Measurements on the plants sampled from natural stands and controlled experiments showed that male-steriles and their progeny had greater biomass and more flowers per plant than hermaphrodites, though these results varied with the environmental conditions. The hermaphrodites of gynodioecious populations had higher rates of selfing than the hermaphrodite individuals in populations lacking male sterility. Estimates of the inbreeding depression and homozygosity levels were also higher in gynodioecious populations. Variation in these parameters of breeding system and relative heterozygosis among populations may explain why male sterility has a restricted distribution, as theoretical models also predict rather specific conditions for this stable polymorphism. These data suggest that the advantage of male sterility is associated with lowered inbreeding depression. However, the potential ecological resource reallocation to the female function needs to be investigated. The fitness differences observed in this study between male-steriles and hermaphrodites appear inadequate to maintain the nucleo-cytoplasmic male sterility but could account for the observed frequencies (10–20%) of male-steriles in nature if the genetic system has evolved from a cytoplasmic system.     

POPULATION SEX STRUCTURE AND REPRODUCTIVE FITNESS IN GYNODIOECIOUS SIDALCEA MALVIFLORA MALVIFLORA (MALVACEAE)

The spatial distribution of females and hermaphrodites within gynodioecious populations is expected to exert considerable selective pressure on gender fitness through pollen limitation of seed set. If pollen flow is predominantly local, seed set in individual plants may be sensitive to the proximity of pollen donors; pollen limitation of seed set may occur if hermaphrodites are locally rare. Under such circumstances, female fitness will be negatively frequency dependent and hermaphrodite fitness will be positively frequency dependent. Given local seed dispersal, a nonrandom clumped distribution of the genders is expected in gynodioecious populations due to the heritability of gender in gynodioecious species. If gender fitness is frequency dependent, such structure should favor hermaphrodites and select against females. To test this hypothesis, I quantified the distribution of the genders in terms of nearest neighbors and neighborhood sex ratio in two populations of gynodioecious Sidalcea malviflora malviflora. I then measured the effect of neighborhood sex ratio on open-pollinated seed set and pollen limitation in both manipulated and unmanipulated neighborhoods. Results indicate that the genders have a patchy distribution and that both genders are pollen limited and show an increase in seed set with an increase in neighborhood hermaphrodite frequency. The observed population sex structure favors hermaphrodites and disadvantages females. These results highlight the importance that population-level traits can have in determining individual fitness and the evolution of sex ratios in gynodioecious species.     

THE EFFECTS OF POPULATION SIZE AND PLANT DENSITY ON OUTCROSSING RATES IN LOCALLY ENDANGERED SALVIA PRATENSIS

Multilocus outcrossing rates were estimated in natural and experimental populations of Salvia pratensis, an entomophilous, gynodioecious, protandrous perennial. Male steriles were used to check the estimation procedure of outcrossing rates in hermaphrodites. Estimates of outcrossing rates in hermaphroditic plants ranged from 38.2% to 81.8% in natural populations and from 71.5% to 95.5% in experimental populations. No correlations were found between outcrossing rates and population size. However, outcrossing in hermaphrodites was promoted by high plant densities and low frequencies of male steriles. It is argued that effective management to preserve genetic variation in populations of S. pratensis should provide for the maintenance of high plant densities.     

Population genetic structure of the gynodioecious Thymus vulgaris L. (Labiatae) in southern France

In a self-compatible gynodioecious species, the abundance of female plants (which are obligate outcrossers) relative to hermaphrodites (which may self and outcross) may be a critical factor influencing genetic diversity and population structure. In the gynodioecious Thymus vulgaris L., female frequency varies from 5 to 95%, providing a suitable model to examine this issue. In this study, we use allozyme markers to (1) evaluate the relationship between female frequency, genetic diversity and population structure, (2) determine whether females and hermaphrodites vary in heterozygote deficiency and (3) examine whether other factors such as plant density are related to heterozygote deficiency. Twenty three natural populations, with female frequencies ranging from 11 to 92%, were sampled in and around the St-Martin-de-Londres basin in southern France. Based on four polymorphic allozyme loci, we found no significant correlation between female frequency and heterozygote deficiency. A significant (P < 0.05) F_IS value over loci and over populations of 0.11 was detected. The F_IS value per population showed a significant heterozygote deficiency in 11 of the 23 populations. However, no significant difference between female and hermaphrodite F_IS values was found. A significant heterozygote deficiency only occurred in populations of intermediate density. There was little differentiation among populations (F_ST = 0.038) nor among subpopulations within each population. The significant F_IS values are thus mostly due to inbreeding effects. The lack of a correlation between F_IS values and female frequency may be due to outcrossing in hermaphrodites and/or restoration of male fertility which may occur to a greater extent at low female frequency. The similarity of female and hermaphrodite F_IS values indicates that females may occasion high levels of biparental inbreeding.     

Reproductive assurance drives transitions to self-fertilization in experimental <Emphasis Type="Italic">Caenorhabditis elegans</Emphasis>

Background

Evolutionary transitions from outcrossing between individuals to selfing are partly responsible for the great diversity of animal and plant reproduction systems. The hypothesis of `reproductive assurance’ suggests that transitions to selfing occur because selfers that are able to reproduce on their own ensure the persistence of populations in environments where mates or pollination agents are unavailable. Here we test this hypothesis by performing experimental evolution in Caenorhabditis elegans.

Results

We show that self-compatible hermaphrodites provide reproductive assurance to a male-female population facing a novel environment where outcrossing is limiting. Invasions of hermaphrodites in male-female populations, and subsequent experimental evolution in the novel environment, led to successful transitions to selfing and adaptation. Adaptation was not due to the loss of males during transitions, as shown by evolution experiments in exclusively hermaphroditic populations and in male-hermaphrodite populations. Instead, adaptation was due to the displacement of females by hermaphrodites. Genotyping of single-nucleotide polymorphisms further indicated that the observed evolution of selfing rates was not due to selection of standing genetic diversity. Finally, numerical modelling and evolution experiments in male-female populations demonstrate that the improvement of male fitness components may diminish the opportunity for reproductive assurance.

Conclusions

Our findings support the hypothesis that reproductive assurance can drive the transition from outcrossing to selfing, and further suggest that the success of transitions to selfing hinges on adaptation of obligate outcrossing populations to the environment where outcrossing was once a limiting factor.

     

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.