Restricted female function of hermaphrodites in a gynodioecious shrub,Daphne jezoensis (Thymelaeaceae)

Journal of Plant Research - Gynodioecy is the coexistence of hermaphrodites and females in a population. It is supposed to be an intermediate stage in the evolutionary pathway from hermaphroditism...     

Differential costs of reproduction in females and hermaphrodites in a gynodioecious plant

Background and Aims

Plants exhibit a variety of reproductive systems where unisexual (females or males) morphs coexist with hermaphrodites. The maintenance of dimorphic and polymorphic reproductive systems may be problematic. For example, to coexist with hermaphrodites the females of gynodioecious species have to compensate for the lack of male function. In our study species, Geranium sylvaticum, a perennial gynodioecious herb, the relative seed fitness advantage of females varies significantly between years within populations as well as among populations. Differences in reproductive investment between females and hermaphrodites may lead to differences in future survival, growth and reproductive success, i.e. to differential costs of reproduction. Since females of this species produce more seeds, higher costs of reproduction in females than in hermaphrodites were expected. Due to the higher costs of reproduction, the yearly variation in reproductive output of females might be more pronounced than that of hermaphrodites.

Methods

Using supplemental hand-pollination of females and hermaphrodites of G. sylvaticum we examined if increased reproductive output leads to differential costs of reproduction in terms of survival, probability of flowering, and seed production in the following year.

Key Results

Experimentally increased reproductive output had differential effects on the reproduction of females and hermaphrodites. In hermaphrodites, the probability of flowering decreased significantly in the following year, whereas in females the costs were expressed in terms of decreased future seed production.

Conclusions

When combining the probability of flowering and seed production per plant to estimate the multiplicative change in fitness, female plants showed a 56 % and hermaphrodites showed a 39 % decrease in fitness due to experimentally increased reproduction. Therefore, in total, female plants seem to be more sensitive to the cost of reproduction in terms of seed fitness than hermaphrodites.     

Frequency‐dependent fitness in gynodioecious Lobelia siphilitica

Selection is frequency dependent when an individual's fitness depends on the frequency of its phenotype. Frequency‐dependent selection should be common in gynodioecious plants, where individuals are female or hermaphroditic; if the fitness of females is limited by the availability of pollen to fertilize their ovules, then they should have higher fitness when rare than when common. To test whether the fitness of females is frequency dependent, we manipulated the sex ratio in arrays of gynodioecious Lobelia siphilitica. To test whether fitness was frequency dependent because of variation in pollen availability, we compared open‐pollinated and supplemental hand‐pollinated plants. Open‐pollinated females produced more seeds when they were rare than when they were common, as expected if fitness is negatively frequency dependent. However, hand‐pollinated females also produced more seeds when they were rare, indicating that variation in pollen availability was not the cause of frequency‐dependent fitness. Instead, fitness was frequency dependent because both hand‐ and open‐pollinated females opened more flowers when they were rare than when they were common. This plasticity in the rate of anthesis could cause fitness to be frequency dependent even when reproduction is not pollen limited, and thus expand the conditions under which frequency‐dependent selection operates in gynodioecious species.     

Female‐biased size dimorphism in a diapausing caddisfly,Mesophylax aspersus: effect of fecundity and natural and sexual selection

1. The effect of mating success, female fecundity and survival probability associated with intra‐sex variation in body size was studied in Mesophylax aspersus, a caddisfly species with female‐biased sexual size dimorphism, which inhabits temporary streams and aestivates in caves. Adults of this species do not feed and females have to mature eggs during aestivation. 2. Thus, females of larger size should have a fitness advantage because they can harbour more energy reserves that could influence fecundity and probability of survival until reproduction. In contrast, males of smaller size might have competitive advantages over others in mating success. 3. These hypotheses were tested by comparing the sex ratio and body size of individuals captured before and after the aestivation period. The associations between body size and female fecundity, and between mating success and body size of males, were explored under laboratory conditions. 4. During the aestivation period, the sex ratio changed from 1 : 1 to male biased (4 : 1), and a directional selection on body size was detected for females but not for males. Moreover, larger clutches were laid by females of larger size. Finally, differences in mating success between small and large males were not detected. These results suggest that natural selection (i.e. the differential mortality of females associated with body size) together with possible fecundity advantages, are important factors responsible of the sexual size dimorphism of M. aspersus. 5. These results highlight the importance of taking into account mechanisms other than those traditionally used to explain sexual dimorphism. Natural selection acting on sources of variation, such as survival, may be as important as fecundity and sexual selection in driving the evolution of sexual size dimorphism.     

Population size, female fecundity, and sex ratio variation in gynodioecious Plantago maritima

Theory predicts that the sex ratio of gynodioecious populations (in which hermaphrodites and females coexist) will be affected by the relative female fitness of females and hermaphrodites, and by founder events and genetic drift in small populations. We documented the sex ratio and size of 104 populations of the gynodioecious, perennial herb Plantago maritima in four archipelagos in eastern Sweden and western Finland (from latitude 53 to 64 degrees N). The sex ratio varied significantly both among and within archipelagos (range 0-70% females, median 6.3% females). The frequency of females was highest in the northernmost archipelago and lowest in the southernmost archipelago. As predicted, females were more frequently missing from small than from large populations, and the variance in sex ratio increased with decreasing population size. The relative fecundity of female plants (mean seed output per female/mean seed output per hermaphrodite) ranged from 0.43 to 2.16 (median 1.01, n = 12 populations). Among the 12 populations sampled for seed production (four in each of three archipelagos), the frequency of females was positively related to relative fecundity of females and negatively related to population size. The results suggest that the local sex ratio is influenced both by the relative fecundity of females and hermaphrodites and by stochastic processes in small populations.     

Wise flies: a pre‐dispersal seed predator prefers hermaphrodites over females in the gynodioecious Polemonium foliosissimum

1. Oviposition choices can profoundly affect offspring performance. Oviposition decisions of the dipteran pre‐dispersal seed predator, Hylemya sp. (Diptera: Anthomyiidae), when choosing among sex morphs of their host‐plant—Polemonium foliosissimum Hook—were evaluated. Polemonium foliosissimum is gynodioecious, with female and hermaphrodite sex morphs that differ in flower size. 2. It was asked: Do female flies preferentially oviposit on hermaphrodite plants and, if so, are oviposition choices correlated with flower size? Is larval survivorship higher on hermaphrodite plants and, if so, is larval success correlated with flower size? Can the differences in oviposition and/or larval success be explained by slight differences in flowering phenology between the sexes? 3. Hermaphrodite flowers received 45% more Hylemya eggs than females. Although hermaphrodites had larger petals and sepals than females, egg loads were not correlated with petal or sepal size. Larval survival was 30% greater on hermaphrodites than females and higher on plants with larger sepals. However, the difference in sepal area between genders did not fully explain larval survival differences. Egg numbers declined over weeks, but differences in egg loads between the sex morphs were not attributable to a slight phenological delay of females. Larval survival declined over the season; however, larval survival differences between sex morphs were consistent. 4. Hylemya preferentially oviposited on hermaphrodites where their larvae had a significantly greater survival rate compared with females. The present results add to the knowledge that intra‐specific choices have consequences for phytophagous insects and that the relationship between antagonists and their gynodioecious host plants is complex.     

Sex‐biased dispersal: a review of the theory

Dispersal is ubiquitous throughout the tree of life: factors selecting for dispersal include kin competition, inbreeding avoidance and spatiotemporal variation in resources or habitat suitability. These factors differ in whether they promote male and female dispersal equally strongly, and often selection on dispersal of one sex depends on how much the other disperses. For example, for inbreeding avoidance it can be sufficient that one sex disperses away from the natal site. Attempts to understand sex‐specific dispersal evolution have created a rich body of theoretical literature, which we review here. We highlight an interesting gap between empirical and theoretical literature. The former associates different patterns of sex‐biased dispersal with mating systems, such as female‐biased dispersal in monogamous birds and male‐biased dispersal in polygynous mammals. The predominant explanation is traceable back to Greenwood's ( 1980 ) ideas of how successful philopatric or dispersing individuals are at gaining mates or the resources required to attract them. Theory, however, has developed surprisingly independently of these ideas: models typically track how immigration and emigration change relatedness patterns and alter competition for limiting resources. The limiting resources are often considered sexually distinct, with breeding sites and fertilizable females limiting reproductive success for females and males, respectively. We show that the link between mating system and sex‐biased dispersal is far from resolved: there are studies showing that mating systems matter, but the oft‐stated association between polygyny and male‐biased dispersal is not a straightforward theoretical expectation. Here, an important understudied factor is the extent to which movement is interpretable as an extension of mate‐searching (e.g. are matings possible en route or do they only happen after settling in new habitat – or can females perhaps move with stored sperm). We also point out other new directions for bridging the gap between empirical and theoretical studies: there is a need to build Greenwood's influential yet verbal explanation into formal models, which also includes the possibility that an individual benefits from mobility as it leads to fitness gains in more than one final breeding location (a possibility not present in models with a very rigid deme structure). The order of life‐cycle events is likewise important, as this impacts whether a departing individual leaves behind important resources for its female or male kin, or perhaps both, in the case of partially overlapping resource use.     

Sex‐biased breeding dispersal is predicted by social environment in birds

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.     

Person (mis)perception: functionally biased sex categorization of bodies

Social perception is among the most important tasks that occur in daily life, and perceivers readily appreciate the social affordances of others. Here, we demonstrate that sex categorizations are functionally biased towards a male percept. Perceivers judged body shapes that varied in waist-to-hip ratio to be men if they were not, in reality, exclusive to women, and male categorizations occurred more quickly than female categorizations (studies 1 and 4). This pattern was corroborated when participants identified the average body shapes of men and women (study 2) and when we assessed participants'' cognitive representations (study 3). Moreover, these tendencies were modulated by emotion context (study 4). Thus, male categorizations occurred readily and rapidly, demonstrating a pronounced categorization bias and temporal advantage for male judgements.     

Sex,reproductive cycle and variations in the fecundity of the family schilbeidae (Osteichthyes : Siluriformes) in Lake Kainji,Nigeria.

The sex, reproductive cycle and variations in the fecundity of the family Schilbeidae (Osteichthyes : Siluriformes) in Lake Kainji, were investigated. Sexual differences in size and morphology were found to exist in all species. Sex ratio varied with species and season. There were more females than males in the population. Size at maturity varied from species to species with the males attaining maturity at a slightly lower length than the females. Breeding condition was attained mainly during the rains in Eutropius niloticus, Schilbe mystus and Siluranodon auritus and in the dry and rainy seasons in Physailia pellucida. Spawning occurred once during the breeding season in E. niloticus and S. mystus; and more than once during the prolonged breeding season in P. pellucida. Condition factors did not show any correlation with maturation of gonads. Fecundity was found to vary from species to species.     

Brain morphology in children with 47,XYY syndrome: a voxel‐ and surface‐based morphometric study

The neurocognitive and behavioral profile of individuals with 47,XYY is increasingly documented; however, very little is known about the effect of a supernumerary Y‐chromosome on brain development. Establishing the neural phenotype associated with 47,XYY may prove valuable in clarifying the role of Y‐chromosome gene dosage effects, a potential factor in several neuropsychiatric disorders that show a prevalence bias toward males, including autism spectrum disorders. Here, we investigated brain structure in 10 young boys with 47,XYY and 10 age‐matched healthy controls by combining voxel‐based morphometry (VBM) and surface‐based morphometry (SBM). The VBM results show the existence of altered gray matter volume (GMV) in the insular and parietal regions of 47,XYY relative to controls, changes that were paralleled by extensive modifications in white matter (WM) bilaterally in the frontal and superior parietal lobes. The SBM analyses corroborated these findings and revealed the presence of abnormal surface area and cortical thinning in regions with abnormal GMV and WMV. Overall, these preliminary results demonstrate a significant impact of a supernumerary Y‐chromosome on brain development, provide a neural basis for the motor, speech and behavior regulation difficulties associated with 47,XYY and may relate to sexual dimorphism in these areas .     

Exploring the genetic basis and proximate causes of female fertility advantage in gynodioecious Thymus vulgaris

In many gynodioecous species, females produce more viable seeds than hermaphrodites. Knowledge of the relative contribution of inbreeding depression in hermaphrodites and maternal sex effects to the female fertility advantage and the genetic basis of variation in female fertility advantage is central to our understanding of the evolution of gender specialization. In this study we examine the relative contribution of inbreeding and maternal sex to the female fertility advantage in gynodioecious Thymus vulgaris and quantify whether there is genetically based variation in female fertility advantage for plants from four populations. Following controlled self and outcross (sib, within-population, and between-population) pollination, females had a more than twofold fertility advantage (based on the number of germinating seeds per fruit), regardless of the population of origin and the type of pollination. Inbreeding depression on viable seed production by hermaphrodites occurred in two populations, where inbreeding had been previously detected. Biparental inbreeding depression on viable seed production occurred in three of four populations for females, but in only one population for hermaphrodites. Whereas the maternal sex effect may consistently enhance female fertility advantage, inbreeding effects may be limited to particular population contexts where inbreeding may occur. A significant family x maternal sex interaction effect on viable seed production was observed, illustrating that the extent of female fertility advantage varies significantly among families. This result is due to greater variation in hermaphrodite (relative to female) seed fertility between families. Despite this genetic variation in female fertility advantage and the highly female biased sex ratios in populations of T. vulgaris, gynodioecy is a stable polymorphism, suggesting that strong genetic and/or ecological constraints influence the stability of this polymorphism.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Sexual differences in response to simulated herbivory in the gynodioecious herb <Emphasis Type="Italic">Geranium sylvaticum</Emphasis>

Several factors have been proposed to explain female maintenance in gynodioecious populations. In this study, we propose and test a novel hypothesis: greater tolerance to herbivory through more beneficial interactions with plant fungal mutualists might also help to explain female maintenance. Herbivory limits the amount of carbon and nutrients available for the plants and has been shown to affect mycorrhizal colonization. We hypothesized that simulated herbivory would decrease reproductive output, mycorrhizal colonization intensity, and the phosphorus content relatively more in hermaphrodites, so females would achieve higher advantage over hermaphrodites when under herbivory pressure. We tested it in the field using the gynodioecious plant Geranium sylvaticum. We found that simulated herbivory had a negative effect on the reproductive output in both sexes and that there was a similar reduction in fruit set, seed set, and total seed number in both sexes. Defoliation did not affect any fungal parameter measured, but decreased phosphorus content relatively more in females. The plants had a sex-specific relationship with mycorrhizae, but this was not related to herbivory. Thus, we conclude that females do not gain any specific advantage under defoliation from its symbionts at short-term even though it seems that the plants have sex-specific relationship with their mycorrhizal symbionts.     

Field evidence challenges the often‐presumed relationship between early male maturation and female‐biased sexual size dimorphism

Female‐biased sexual size dimorphism (SSD) is often considered an epiphenomenon of selection for the increased mating opportunities provided by early male maturation (i.e., protandry). Empirical evidence of the adaptive significance of protandry remains nonetheless fairly scarce. We use field data collected throughout the reproductive season of an SSD crab spider, Mecaphesa celer, to test two hypotheses: Protandry provides fitness benefits to males, leading to female‐biased SSD, or protandry is an indirect consequence of selection for small male size/large female size. Using field‐collected data, we modeled the probability of mating success for females and males according to their timing of maturation. We found that males matured earlier than females and the proportion of virgin females decreased abruptly early in the season, but unexpectedly increased afterward. Timing of female maturation was not related to clutch size, but large females tended to have more offspring than small females. Timing of female and male maturation was inversely related to size at adulthood, as early‐maturing individuals were larger than late‐maturing ones, suggesting that both sexes exhibit some plasticity in their developmental trajectories. Such plasticity indicates that protandry could co‐occur with any degree and direction of SSD. Our calculation of the probability of mating success along the season shows multiple male maturation time points with similar predicted mating success. This suggests that males follow multiple strategies with equal success, trading‐off access to virgin females with intensity of male–male competition. Our results challenge classic hypotheses linking protandry and female‐biased SSD, and emphasize the importance of directly testing the often‐assumed relationships between co‐occurring animal traits.     

Biased sex‐ratio and sex‐biased heterozygote disadvantage affect the maintenance of a genetic polymorphism and the properties of hybrid zones

The evolution of biodiversity is a major issue of modern biology, and it is becoming increasingly topical as the ongoing erosion of diversity puts serious threats on human well‐being. An elementary mechanism that allows maintaining diversity is the interplay between dispersal and heterozygote selective disadvantage, which can lead to self‐sustainable spatial genetic structures and is central to the stability of hybrid zones. Theoretical studies supporting the importance of this mechanism assume a balanced sex‐ratio and a heterozygote disadvantage equally affecting both sexes, despite the multiplicity of empirical evidence that (i) adult sex‐ratio is usually biased towards either male or female and that (ii) heterozygote disadvantage often affects a single sex. We expanded the existing theory by weighting the strength of selection against heterozygote according to the biased in sex‐ratio and in heterozygote disadvantage. The range of conditions allowing for the maintenance of polymorphism can then either double or vanish. We discuss the implications of such finding for birds, mammals and insects diversity. Finally, we provide simple analytical predictions about the effect of those biased on the width and speed of hybrid zones and on the time for the spread of beneficial mutations through such zones.     

Within‐population Y‐linked genetic variation for lifespan in Drosophila melanogaster

The view that the Y chromosome is of little importance for phenotypic evolution stems from early studies of Drosophila melanogaster. This species’ Y chromosome contains only 13 protein‐coding genes, is almost entirely heterochromatic and is not necessary for male viability. Population genetic theory further suggests that non‐neutral variation can only be maintained at the Y chromosome under special circumstances. Yet, recent studies suggest that the D. melanogaster Y chromosome trans‐regulates hundreds to thousands of X and autosomal genes. This finding suggests that the Y chromosome may play a far more active role in adaptive evolution than has previously been assumed. To evaluate the potential for the Y chromosome to contribute to phenotypic evolution from standing genetic variation, we test for Y‐linked variation in lifespan within a population of D. melanogaster. Assessing variation for lifespan provides a powerful test because lifespan (i) shows sexual dimorphism, which the Y is primarily predicted to contribute to, (ii) is influenced by many genes, which provides the Y with many potential regulatory targets and (iii) is sensitive to heterochromatin remodelling, a mechanism through which the Y chromosome is believed to regulate gene expression. Our results show a small but significant effect of the Y chromosome and thus suggest that the Y chromosome has the potential to respond to selection from standing genetic variation. Despite its small effect size, Y‐linked variation may still be important, in particular when evolution of sexual dimorphism is genetically constrained elsewhere in the genome.     

雌雄异株植物鼠李的生殖分配

以雌雄异株树种鼠李为模式物种,分别从树枝、植株和种群水平上分析了雌雄异株树种鼠李的生殖分配过程,检验了营养生长与生殖过程之间的平衡。结果表明:树枝水平,鼠李年生殖生物量(花生物量+果生物量)投资具有显著的性别差异和个体差异(P<0.001)。雌花生物量大于雄花生物量,雌花生物量最大值为雄花生物量最大值的1.75倍。雌树和雄树的叶片生物量差异不显著(P>0.05)。植株水平上,鼠李生殖生物量(花生物量+果生物量)投资具有显著的性别差异和个体差异(P<0.001),雌树与雄树的花生物量和茎干径向增量差异显著(P<0.05),叶片生物量差异不显著(P>0.05)。鼠李胸径大小对花生物量、叶生物量和茎干径向增量影响显著(P<0.05)。鼠李雌树的花生物量和茎干径向增量均大于雄树。种群水平上,鼠李雄树始花期略早于雌树,2010年雌树和雄树分别于5月28日和5月25日始花。在360 m × 660 m研究样地内种群性比为0.17,卡方检验表明种群性比显著偏离1∶1(P<0.001)。雌树和雄树年平均生长量分别为0.78 mm和0.83 mm。因此,在树枝水平、植株水平以及种群水平上,雌雄异株树种鼠李的营养生长和生殖生长不存在平衡关系。推断鼠李雌树能够通过光合过程获得更多生物量来满足其生殖和营养生长过程需要。     

Male‐specific mortality biases secondary sex ratio in Eurasian tree sparrows Passer montanus

Sex allocation theory predicts that parents bias the offspring sex ratio strategically. In avian species, the offspring sex ratio can be biased at multiple growth stages, although the mechanisms are not well known. It is crucial to reveal a cause and timing of biased offspring sex ratio. We investigated (i) offspring sex ratio at multiple growth stages, from laying to fledging; and (ii) the stage at which offspring sex ratio became biased; and (iii) the cause of biased offspring sex ratio in Eurasian tree sparrows Passer montanus. Sex determination of 218 offspring, including hatchlings and unhatched eggs from 41 clutches, suggested that the offspring sex ratio was not biased at the egg‐laying stage but was significantly female‐biased after the laying stage due to higher mortality of male embryos. Half of the unhatched eggs showed no sign of embryo development (37/74, 50.00%), and most undeveloped eggs were male (36/37, 97.30%). Additional experiments using an incubator suggested that the cause of embryo developmental failure was a lack of developmental ability within the egg, rather than a failure of incubation. This study highlights the importance of clarifying offspring sex ratio at multiple stages and suggests that offspring sex ratio is adjusted after fertilization.