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.     

The effects of sex ratio and density on the expression of gender in the polychaeteCapitella capitata

Summary Large natural populations of the marine polychaeteCapitella capitata (species type I) contain males, females, and occasionally, hermaphrodites. Environmental conditions control the occurrence of hermaphrodites. At low density or in groups with female-biased sex ratios, males develop into hermaphrodites, and hermaphrodites are common. Crosses suggest that females are heterogametic, and males and hermaphrodites are homogametic. Heterogametic females do not become hermaphrodites.This study shows that in homogametic individuals, environmental conditions determine not only the development of hermaphroditism but also the expression of initial gender. Homogametic individuals can express either male or female gender initially, and homogametic individuals of either gender can develop subsequently into simultaneous hermaphrodites. The choice of initial gender depends on isolation. Most homogametic juveniles become females if reared alone but males if reared with other conspecifics. Homogametic males readily develop into hermaphrodites if females are rare. In contrast, homogametic females rarely become hermaphrodites.     

Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae)

Polygamy (including trioecy and subdioecy), the co-occurrence of males, hermaphrodites, and females in natural populations, is a rare and poorly studied breeding system expressed in Fraxinus excelsior L. (Oleaceae), a wind-pollinated tree. Here we investigate siring ability of pollen from male vs. hermaphrodite individuals to better understand this sex polymorphism. We conducted single-donor and two-donor pollination experiments and compared both fruit set and seed siring success, assessed with polymorphic microsatellite markers, of male and hermaphrodite individuals. Single pollen donor crosses allowed us to verify the male function of hermaphrodites. However, pollen from hermaphrodites was much less proficient than male pollen, with males siring 10 times as many fruits in single donor pollination treatments. This result was strengthened by the surprisingly low reproductive success of hermaphrodites in pollen competition conditions: of the 110 seedlings analyzed three were selfed and only one was sired by the hermaphrodite donor. The remaining 106 were sired by the male pollen donor. These results raise the question of the maintenance of male fertility in hermaphrodites in Fraxinus excelsior. Male function of hermaphrodites in this species now needs to be assessed under field conditions.     

Population dynamics of species with gynogenetic sibling species

Models are formulated for the population dynamics of a monoecious or dioecious species with an all-female parthenogenetic sibling species which is also gynogenetic. Continuous, deterministic reproduction and mortality, a stationary age distribution, random mating, and limited sexual competence for all individuals are posited. It is also supposed that in the dioecious case males do not distinguish between true and gynogenetic females. Similarly, hermaphrodites do not differentiate hermaphrodites and gynogens. The model implies that extinction is highly likely in the dioecious situation, but much less so in the monoecious one. Empirical evidence is reviewed and related to the assumptions and conclusions.     

Sequential hermaphroditism and personality in a clonal vertebrate: the mangrove killifish

Individuals are regularly documented to consistently differ in their behavioural types (BTs). For example, some individuals are bold whereas others are shy. Within the human personality literature, the big five personality dimensions are commonly documented to be sex-specific with testosterone suggested to underpin traits such as aggressiveness. In non-human animals recent research suggests sex-specific BT expression may be influenced by ecology, mating system and sexual selection. While most research on sex-specific personality has focused on dioecious species, we explore sex differences in BT expression in a sequential hermaphrodite the mangrove killifish. We replicate within 7 isogenic genotypes and investigate sex differences (hermaphrodite and secondary male) in three BTs (exploration, boldness and aggression). This approach allows us to investigate sex differences in BT expression whilst controlling for genetic variation. In this study we find that both secondary males and hermaphrodites are repeatable at the individual level yet there was no difference between the sexes in average BT scores. Furthermore, aggression scores differed between genotypes, and were repeatable at the genotype level, suggesting strong genetic control. Finally, male boldness was significantly more repeatable than hermaphrodites potentially supporting recent proposals relating to sexual selection. We document a behavioural syndrome in male fish with bolder individuals being more aggressive, this behavioural syndrome was not observed however in hermaphrodites. In contrast to a previous developmental study in this species exploration did not correlate with either aggression or boldness in either males or hermaphrodites.     

Sexual selection and simultaneous hermaphroditism among the Unionidae (Bivalvia: Mollusca)

Simultaneous hermaphroditism is an infrequent mode of reproduction among bivalves of the family Unionidae: only five of the 220 North American species are simultaneous hermaphrodites. However, hermaphroditic individuals of otherwise predominantly dioecious species have been encountered in 30 of I01 species examined. These hermaphroditic individuals as well as simultaneous hermaphrodites can exhibit considerable variability in the ratio of spermatogenic: oogenic tissue within the gonad, and the purposes of this paper are to determine the underlying causes of both this variability and the occurrence of occasional hermaphroditic individuals among dioecious species. Results indicate that the ratio of male: female gonodal tissue of a simultaneous hermaphrodite is bimodally distributed, and several hypotheses to account for this observation are presented. It is proposed that populations occurring in different habitats and under conditions of different individual density are subject to fundamentally different sexual selection pressures acting on ratios of allocation to male and female gametes. Occasional hermaphroditism among otherwise predominantly dioecious species was in this study associated with infection of the gonads by digenean trematodes. A model of sexual determination among unionids presented in this paper proposes that sex is determined by genetically controlled hormone levels: occasional hermaphrodites result from alterations in these hormone levels caused by developmental errors and trematodal infections which mimic the results of such errors. Predictions of this model are consistent with observed levels of variability in male: females gonadal tissue among occasional hermaphrodites.     

High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia

Androdioecy, the coexistence of males and hermaphrodites within a population, is a rare breeding system, often considered as unlikely to evolve because of restrictive conditions for its maintenance. Phillyrea angustifolia, a wind-pollinated shrub, is one of the handful species reported to be androdioecious. Our previous studies have shown that natural populations of this species in southern France exhibit higher male frequencies (approximately 50%) than predicted on theoretical grounds. Thus, the male functionality of hermaphrodites is still debated. To assess the functional breeding system of this species in the wild, a paternity analysis was performed with two highly polymorphic microsatellite loci on 729 seeds collected on 10 maternal shrubs in a natural population of 24 mature individuals of P. angustifolia. A large proportion of seeds were found to have been sired by pollen from outside the population. Analysis of seeds sired by individuals within the study population revealed a high male fertility of hermaphrodites resulting in a low male advantage in fertility for male plants. Intermate distances were found to have a strong impact on male reproductive success, whereas sexual morph had no effect, with males and hermaphrodites performing equivalently. This study is the first to unequivocally document the occurrence of a male function of hermaphrodites in a natural population of an androdioecious species.     

Variation in reproductive success and gonadal allocation in the simultaneous hermaphrodite,Serranus fasciatus

Summary This paper examines the correlates of individual size, reproductive success, gonadal allocation, and growth in a hermaphroditic reef fish. Individuals in S. fasciatus mature as simultaneous hermaphrodites; large individuals subsequently lose female function and become functional males. Daily female reproductive success was highly correlated with both hermaphrodite size and amount of female gonadal tissue. Three separate comparisons gave a positive correlation between male reproductive success and male gonadal allocation: (1) Males had higher levels of male gonadal allocation and male reproductive success than hermaphrodites. (2) The percent of gonad allocated to male tissue in hermaphrodites was higher in the year they had higher male mating success. (3) Male gonadal tissue of hermaphrodites was positively correlated with male reproductive success in the year that male reproductive success by hermaphrodites was higher and more variable. There was no evidence for a trade-off between male function, female function, and growth among hermaphrodites. Many of these patterns have also been observed in plants, but the selective pressures leading to these patterns in S. fasciatus and plants are probably quite different.     

Evolution: vertebrate reproductive strategies get mixed up

The mangrove killifish is the only vertebrate known to have a mixed-mating strategy, where hermaphrodites reproduce by either self-fertilisation or cross-breeding. New molecular evidence from this species reveals that occasional cross-breeding between common hermaphroditic individuals and rare pure males results in an injection of genetic variation into otherwise highly homozygous 'clonal' lineages.     

Density-dependent regulation of the sex ratio in an annual plant

Sex ratios are subject to strong frequency-dependent selection regulated by the mating system and the relative male versus female investment. In androdioecious plant populations, where males co-occur with hermaphrodites, the sex ratio depends on the rate of self-fertilization by hermaphrodites and on the relative pollen production of males versus hermaphrodites. Here, we report evolutionary changes in the sex ratio from experimental mating arrays of the androdioecious plant Mercurialis annua. We found that the progeny sex ratio depended strongly on density, with fewer males in the progeny of plants grown under low density. This occurred in part because of a plastic adjustment in pollen production by hermaphrodites, which produced more pollen when grown at low density than at high density. Our results provide support for the prediction that environmental conditions govern sex ratios through their effects on the relative fertility of unisexual versus hermaphrodite individuals.     

Disentangling the causes of heterogeneity in male fecundity in gynodioecious Beta vulgaris ssp. maritima

Variation among individuals in reproductive success is advocated as a major process driving evolution of sexual polymorphisms in plants, such as gynodioecy where females and hermaphrodites coexist. In gynodioecious Beta vulgaris ssp. maritima, sex determination involves cytoplasmic male sterility (CMS) genes and nuclear restorers of male fertility. Both restored CMS and non-CMS hermaphrodites co-occur. Genotype-specific differences in male fitness are theoretically expected to explain the maintenance of cytonuclear polymorphism. Using genotypic information on seedlings and flowering plants within two metapopulations, we investigated whether male fecundity was influenced by ecological, phenotypic and genetic factors, while taking into account the shape and scale of pollen dispersal. Along with spatially restricted pollen flow, we showed that male fecundity was affected by flowering synchrony, investment in reproduction, pollen production and cytoplasmic identity of potential fathers. Siring success of non-CMS hermaphrodites was higher than that of restored CMS hermaphrodites. However, the magnitude of the difference in fecundity depended on the likelihood of carrying restorer alleles for non-CMS hermaphrodites. Our results suggest the occurrence of a cost of silent restorers, a condition supported by scarce empirical evidence, but theoretically required to maintain a stable sexual polymorphism in gynodioecious species.     

Testing for sex differences in biparental inbreeding and its consequences in a gynodioecious species

In many gynodioecious species cross-pollinated seeds from females outperform those from hermaphrodites. Using the gynodioecious alpine perennial Silene acaulis, I investigated whether this was the result of greater biparental inbreeding among hermaphrodites leading to greater biparental inbreeding depression. I also determined the influence of relatedness on progeny fitness. Experiments were performed using individuals from a site whose population structure and coefficient of inbreeding was known. In the first experiment, crosses were made on plants in the field to determine the effect of seven different crossing distances, plus selfing, on germination and early seedling survival and growth. Although selfed seeds died more often and grew slower than crossed seeds, the effect of crossing distance was negligible for all measured fitness traits, refuting the biparental inbreeding hypothesis as a mechanism to explain why seeds from hermaphrodites die more often than those from females. Nonetheless, cross-pollinated seeds from hermaphrodites did die more, indicating that another mechanism must be responsible. In the second experiment, the effect of different levels of inbreeding on germination and seedling survival was determined by growing seeds from experimental matings varying in relatedness. Inbreeding depression for a multiplicative fitness estimate was significant for all levels of inbreeding, suggesting that inbred individuals are unlikely to become established in the population and providing insight into the results of the first experiment. Alternative hypotheses are discussed to explain why seeds from hermaphrodites die more often, which together with the results of this study, suggest that the restoration of male function in hermaphrodites comes with a correlated cost to seedling survival.     

Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp

Protandric simultaneous hermaphroditism, as reported for shrimps in the genus Lysmata, is a sexual system in which individuals invariably reproduce as males first and later in life as simultaneous hermaphrodites. I tested three models (i.e., sex-dependent energetic costs, sex-dependent mortality rates and sex-dependent time commitments) in an attempt to explain the adaptive value of protandric simultaneous hermaphroditism in the shrimp L. wurdemanni. Specific assumptions and predictions of each model were evaluated using manipulative experiments. In the laboratory, males grew faster than simultaneous hermaphrodites of the same size and age, an indication that the female function incurs higher energetic costs of reproduction than the male function. Also, large SHPs were more successful in monopolizing food than small males. The sex-dependent growth rate and size-dependent resource holding power agree with predictions of the sex-dependent energetic cost model. The time that simultaneous hermaphrodites required for replenishing their sperm reservoirs after mating as males was much shorter (2 days) than the time required to brood one clutch of embryos (11 days). Also, small simultaneous hermaphrodites experienced heavier mortality due to predatory fishes than large ones. The sex-dependent reproductive time commitment and size-dependent mortality agree with predictions of the sex-dependent time commitment model. Conversely, I found no evidence that the sex-dependent mortality model explains protandric simultaneous hermaphroditism in the studied species. In contrast to model predictions, mortality due to predatory fishes suffered by simultaneous hermaphrodites was not greater than that suffered by males of the same body size. In L. wurdemanni, the relationship between sex-specific investment and reproductive success seems to change during ontogeny in a way that is consistent with an adaptive adjustment of sex allocation to improve age-specific reproductive success.     

Sex expression,female frequency,and reproductive output in a gynodioecious clonal herb, <Emphasis Type="Italic">Glechoma longituba</Emphasis> (Lamiaceae)

We investigated the sex morphs and frequency of females in 24 natural populations of the clonal, gynodioecious species Glechoma longituba. In addition to the presence of hermaphrodites and females, there were some individuals with intermediate sex expression that could not be categorized as either morph. The majority of populations contained a predominance of hermaphrodites, although female frequency varied from 0 to 100%. The sexual expression of individual ramets did not change over three consecutive years or when ramets were transplanted to different populations, but it did change over the course of a flowering season. Seeds from females weighed more than those from hermaphrodites. The seed set of hermaphrodites was relatively constant across populations; the seed set of females was higher than that of hermaphrodites in most populations, but lower in populations in which females occurred at a very high frequency because of pollen limitation. This led to a negative correlation being detected between the seed set of females and the frequency of females in a population. We postulated that the adjustment of sex expression within seasons could be an adaptive mechanism of reproductive assurance in this system.     

Sex‐specific reproductive components and pollination ecology in the subdioecious shrub Fuchsia microphylla

In subdioecious populations, functional female, male and hermaphrodite individuals coexist. Subdioecy may be a transitional state towards dioecy or a breakdown of dioecy, although lability in sex expression may maintain subdioecy as a stable condition. To better understand the ecological aspects involved in sex ratio dynamics and breeding system evolution, we studied the pollination and female fitness components of female and hermaphrodite individuals of the subdioecious shrub Fuchsia microphylla. In two natural populations at the Trans‐Mexican Volcanic Belt we estimated female frequency and several reproductive components of female and hermaphrodite plants under natural pollination and experimental pollination treatments. Average female frequency was 42%, and on average, 42.5% of hermaphrodites produced fruits. Female plants showed a 17‐fold female fertility advantage over hermaphrodites through increased fruit production, as the number of seeds and germination rates did not differ between morphs. Hermaphrodite flowers were larger, with similar nectar production and concentration to female flowers, and pollinators did not show consistent morph preferences. Some hermaphrodites produced fruits autonomously, and female flowers excluded from pollinators produced fruits putatively by apomixis. Fruit production in hermaphrodites, but not in females, was related to height, suggesting increased investment of hermaphrodites in the female function at higher resource status. For sex ratios to be at equilibrium, the female fertility advantage should be reduced about eightfold. However, it may be that hermaphrodites are maintained by producing fruits at no cost to the male function at higher resource status, as the gender plasticity hypothesis proposes.     

Sex-differential herbivory in androdioecious Mercurialis annua

Males of plants with separate sexes are often more prone to attack by herbivores than females. A common explanation for this pattern is that individuals with a greater male function suffer more from herbivory because they grow more quickly, drawing more heavily on resources for growth that might otherwise be allocated to defence. Here, we test this 'faster-sex' hypothesis in a species in which males in fact grow more slowly than hermaphrodites, the wind-pollinated annual herb Mercurialis annua. We expected greater herbivory in the faster-growing hermaphrodites. In contrast, we found that males, the slower sex, were significantly more heavily eaten by snails than hermaphrodites. Our results thus reject the faster-sex hypothesis and point to the importance of a trade-off between defence and reproduction rather than growth.     

Spatial and temporal patterns of size-at-sex-change in two exploited coastal fish

Fisheries are known to selectively remove larger and older individuals from wild populations. In sequential hermaphrodites, size-selectivity also becomes ‘sex-selectivity’, as the largest and oldest individuals of a sex-changing population primarily belong to one sex. Plasticity in size-at-sex-change is believed to circumvent the undesirable effects of gamete limitation and low effective population size. Here we present data of two commercially exploited sea bream species in different biogeographic regions, one protandrous (male-first) and one protogynous (female-first), respectively exhibiting spatial and temporal fluctuation in size-at-sex-change. By contrasting the patterns found against recent evidence of similar phenomena in other species, we discuss life-history strategies that favour reproductive success in different environmental scenarios. Size-at-sex-change may be for sequential hermaphrodites as important a life-history parameter as size-at-maturity or age-at-size. Consequently, the demographic consequences of altered size-at-sex-change should be considered explicitly in stock management and assessment.     

Female reproductive success in gynodioecious Thymus vulgaris: pollen versus nutrient limitation and pollinator foraging behaviour

Gynodioecy is a dimorphic breeding system in which female individuals coexist with hermaphroditic individuals in the same population. Females only contribute to the next generation via ovules, and many studies have shown that they are usually less attractive than hermaphrodites to pollinators. Several mechanisms have been proposed to explain how females manage to persist in populations despite these disadvantages. The ‘resource reallocation hypothesis’ (RRH) states that females channel resources not invested in pollen production and floral advertisement towards the production of more and/or larger seeds. We investigated pollination patterns and tested the RRH in a population of Thymus vulgaris. We measured flower display, flower size, nectar production, visitation rates, pollinator constancy and flower lifespan in the two morphs. In addition, we measured experimentally the effects of pollen and resource addition on female reproductive success (fruit set, seed set, seed weight) of the two morphs. Despite lower investment in floral advertisement, female individuals were no less attractive to pollinators than hermaphrodites on a per flower basis. Other measures of pollinator behaviour (number of flowers visited per plant, morph preference and morph constancy) also showed that pollinators did not discriminate against female flowers. In addition, stigma receptivity was longer in female flowers. Accordingly, and contrary to most studies on gynodioecious species, reproductive success of females was not pollen limited. Instead, seed production was pollen limited in hermaphrodites, suggesting low levels of cross‐pollination in hermaphrodites. Seed production was resource limited in hermaphrodites, but not in females, thus providing support for the RRH. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175 , 395–408.     

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.