Sex-different response in growth traits to resource heterogeneity explains male-biased sex ratio

In dioecious plants, differences in growth traits between sexes in a response to micro-environmental heterogeneity may affect sex ratio bias and spatial distributions. Here, we examined sex ratios, stem growth traits and spatial distribution patterns in the dioecious clonal shrub Aucuba japonica var. borealis, in stands with varying light intensities. We found that male stems were significantly more decumbent (lower height/length ratio) but female stems were upright (higher height/length ratio). Moreover, we found sex-different response in stem density (no. of stems per unit area) along a light intensity gradient; in males the stem density increased with increases in canopy openness, but not in females. The higher sensitivity of males in increasing stem density to light intensity correlated with male-biased sex ratio; fine-scale sex ratio was strongly male-biased as canopy openness increased. There were also differences between sexes in spatial distributions of stems. Spatial segregation of sexes and male patches occupying larger areas than female patches might result from vigorous growth of males under well-lit environments. In summary, females and males showed different growth responses to environmental variation, and this seemed to be one of possible causes for the sex-differential spatial distributions and locally biased sex ratios.     

Spatial sex segregation in the dioecious grass Poa ligularis in northern Patagonia: the role of environmental patchiness

We examined the effect of environmental patchiness on the spatial segregation of the sexes in the dioecious anemophilus grass Poa ligularis. Because the species is sensitive to grazing, a better understanding of environmental factors that control its spatial distribution and abundance could improve conservation efforts. We hypothesized that (i) males and females are spatially segregated in the microenvironments created by plant patches as the result of sexual specialization in habitat and/or resources use, (ii) sexual specialization is related to different tolerance to competition and reproductive costs of males and females, and (iii) changes in patch structure affect the microenvironment and the intensity of spatial segregation of the sexes. We analyzed the spatial distribution of sexes at three sites with different plant and micro-environmental patchiness and performed a controlled competition experiment with different substitution of males and females. Our results showed that large plant patches created larger sheltered soil fertility islands than small patches. As patch size and their area of influence increased, the density and the spatial segregation of the sexes of P. ligularis also increased, resulting in biased habitat-specific sex ratios. In accordance with their higher reproductive costs, females were more frequent in sheltered (low air evaporative demand) and nitrogen-rich areas inside patch perimeters than males. Females were also better able to tolerate inter-sexual competition than males. In contrast, males tolerated low nitrogen concentration in soil and low sheltering, probably gaining advantage in pollen dispersal. Inter- and intra-sexual competition, however, affected the reproductive output of both sexes. From the point of view of conservation, environmental patchiness is important to the status of P. ligularis populations. The reduction of patch size limits the available microsites, biases the sex ratio towards males inside patches, increases inter- and intra-sexual competition, and it might be expected to decrease overall seed and pollen production and consequently potential recruitment.     

Sex ratio at mating does not modulate age fitness effects in Drosophila melanogaster

Understanding the effects of male and female age on reproductive success is vital to explain the evolution of life history traits and sex‐specific aging. A general prediction is that pre‐/postmeiotic aging processes will lead to a decline in the pre‐ and postcopulatory abilities of both males and females. However, in as much the sexes have different strategies to optimize their fitness, the decline of reproductive success late in life can be modulated by social context, such as sex ratio, in a sex‐specific manner. In this study, we used Drosophila melanogaster to investigate whether sex ratio at mating modulates age effects on male and female reproductive success. As expected, male and female age caused a decrease in reproductive success across male‐biased and female‐biased social contexts but, contrary to previous findings, social context did not modulate age‐related fitness decline in either of the two sexes. We discuss these results in the light of how sex ratio might modulate pre‐/postcopulatory abilities and the opportunity for inter‐ and intrasexual competition in D. melanogaster, and generally suggest that social context effects on these processes are likely to be species specific.     

Females make tough neighbors: sex-specific competitive effects in seedlings of a dioecious grass

If males and females of a species differ in their effect on intraspecific competition then this can have significant ecological and evolutionary consequences because it can lead to size and mortality disparities between the sexes, and thus cause biased population sex ratios. If the degree of sexual dimorphism of competitive effect varies across environments then this variation can generate sex ratio variation within and between populations. In a California population of Distichlis spicata, a dioecious grass species exhibiting extreme within-population sex ratio variation (spatial segregation of the sexes), I evaluated the intraspecific competitive effects of male and female D. spicata seedlings in three soil types. The sex of seedlings was determined using a RAPD-PCR marker co-segregating with female phenotype. Distichlis spicata seedlings, regardless of sex, were six times larger when grown with male versus female conspecific seedlings in soil from microsites where the majority of D. spicata plants are female, and this sexual dimorphism of competitive effect was weaker or did not occur in other soil types. This study suggests that it is not just the higher costs of female versus male reproduction itself that cause spatial segregation of the sexes in D. spicata, but that differences in competitive abilities between the sexes—which occur as early as the seedling stage—can generate sex ratio variation.     

The influence of demography and local mating environment on sex ratios in a wind‐pollinated dioecious plant

Negative frequency‐dependent selection should result in equal sex ratios in large populations of dioecious flowering plants, but deviations from equality are commonly reported. A variety of ecological and genetic factors can explain biased sex ratios, although the mechanisms involved are not well understood. Most dioecious species are long‐lived and/or clonal complicating efforts to identify stages during the life cycle when biases develop. We investigated the demographic correlates of sex‐ratio variation in two chromosome races of Rumex hastatulus, an annual, wind‐pollinated colonizer of open habitats from the southern USA. We examined sex ratios in 46 populations and evaluated the hypothesis that the proximity of males in the local mating environment, through its influence on gametophytic selection, is the primary cause of female‐biased sex ratios. Female‐biased sex ratios characterized most populations of R.  hastatulus (mean sex ratio = 0.62), with significant female bias in 89% of populations. Large, high‐density populations had the highest proportion of females, whereas smaller, low‐density populations had sex ratios closer to equality. Progeny sex ratios were more female biased when males were in closer proximity to females, a result consistent with the gametophytic selection hypothesis. Our results suggest that interactions between demographic and genetic factors are probably the main cause of female‐biased sex ratios in R. hastatulus. The annual life cycle of this species may limit the scope for selection against males and may account for the weaker degree of bias in comparison with perennial Rumex species.     

Sexual differences and sex ratios of dioecious plants under stressful environments

雌雄异株植物对环境胁迫响应的性别差异与性别比例 雌雄异株植物在性特征(繁殖器官)和次级性特征(植物的特征)均表现出性二态。形态、生理与生态特征等次级性特征的性别差异,通常在繁殖成本和其他功能性状之间存在着权衡。尽管有证据表明性二态对环境胁迫的响应不一定存在于所有植物中,但次级性特征的权衡可能受到环境胁迫的影响。当植物表现出性二态时,不同的物种与胁迫因子可以导致性别特异性的响应。因此,胁迫作用对雌雄异株植物影响的概括性研究是必须的。另外,性二态可能会影响雌雄异株植物沿着环境梯度的频率和分布,引起生态位分化与性别空间分异。目前,控制性别比例偏差的原因和机制还知之甚少。本综述旨在讨论不利环境下的性别特异性响应与性别比例偏差,有利于深入的理解性二态对环境胁迫的响应。     

Sex ratio and gender-dependent neighboring effects in <Emphasis Type="Italic">Podocarpus nagi</Emphasis>, a dioecious tree

We analyzed sex ratio, growth rates, and spacing among individuals of Podocarpus nagi, a dioecious tree, on Mt. Mikasa, Nara City, Japan. The sex ratio of reproductive trees ≥ 5 cm in stem diameter at breast height (dbh, 130 cm above ground level) was significantly male-biased. The sex ratio was male-biased in the < 20 cm and ≥ 50 cm size classes, while it did not depart from 1:1 in the 20 ≤ dbh < 50 cm class. Growth rate varied with tree size in males but not in females. The precocity and vigor of males suggests that differences in reproductive costs between sexes induce the biased sex ratio. Random labeling tests on the positions of reproductive trees showed that in the < 30 cm class, males and females were distributed randomly and independently from each other. In the ≥ 30 cm class, males were significantly clumped, whereas females were randomly distributed. Males and females showed significant repulsion, i.e., a spatial segregation of sexes. Both intra- and intersexual effects on the growth rate of crowding by neighbors were significant for females, but not for males. Maximum competitive interference was observed at a distance of 5 m, which corresponded approximately to the radius of clumps of large males and to the significant repulsive distance between large males and females. These results suggest that sexual differences in sensitivity to local crowding are related to the formation of gender-dependent spatial patterns. Formation of female-repulsive male clumps and a male-biased sex ratio may intensify the decreased probability of regeneration near males, as suggested by the limited seed-dispersal range of this species, thereby promoting coexistence with other species.     

Impacts of diet quality on life‐history and reproductive traits in male and female armed beetle,Gnatocerus cornutus

1. The energy available for reproduction is usually limited by resource acquisition (i.e. condition). Because condition is known to be strongly affected by environmental factors, reproductive investments also vary across heterogeneous environments. 2. Although the condition dependence of reproductive investment is common to both sexes, reproductive traits may exhibit sexually different responses to environmental fluctuation due to sex‐specific life‐history strategies. However, few direct experimental studies have investigated the condition dependence of reproductive investments in both sexes. 3. We investigated the condition dependence of life‐history and reproductive traits of males and females in the beetle Gnatocerus cornutus Fabricus by manipulating larval and adult diet quality. We found that male and female life‐history traits exhibited similar responses to environmental fluctuations. 4. By contrast, the sexes exhibit different patterns of condition dependence in reproductive traits (i.e. the adult nutritional environment has a strong impact on the female lifetime reproductive success, whereas larval nutritional environment strongly affects the secondary sexual trait in males). 5. This difference in the plasticity of reproductive traits may lead to different selection pressures for each sex, even if both sexes develop and/or live in the same environment.     

Sex ratio variation and spatial segregation of the sexes in populations ofRumex acetosa andR. acetosella (Polygonaceae)

Populations ofRumex acetosa andR. acetosella were studied during two growth seasons. The ramet sex ratios ofR. acetosa were always female-biased. InR. acetosella the sex ratios expressed more variation but were mostly female-biased. In both species the sex ratios commonly varied between subpopulations reflecting a partial spatial segregation of the sexes. No marked differences between sexes in vegetative vigour were detected in either species. Interactions between sex ratios, various soil characteristics and population densities were determined. Possible mechanisms for causing biased sex ratios and partial spatial segregation of the sexes are discussed.     

Slow evolution of sex‐biased genes in the reproductive tissue of the dioecious plant Salix viminalis

The relative rate of evolution for sex‐biased genes has often been used as a measure of the strength of sex‐specific selection. In contrast to studies in a wide variety of animals, far less is known about the molecular evolution of sex‐biased genes in plants, particularly in dioecious angiosperms. Here, we investigate the gene expression patterns and evolution of sex‐biased genes in the dioecious plant Salix viminalis. We observe lower rates of sequence evolution for male‐biased genes expressed in the reproductive tissue compared to unbiased and female‐biased genes. These results could be partially explained by the lower codon usage bias for male‐biased genes leading to elevated rates of synonymous substitutions compared to unbiased genes. However, the stronger haploid selection in the reproductive tissue of plants, together with pollen competition, would also lead to higher levels of purifying selection acting to remove deleterious variation. Future work should focus on the differential evolution of haploid‐ and diploid‐specific genes to understand the selective dynamics acting on these loci.     

Differential niche modification by males and females of a dioecious herb: extending the Jack Sprat effect

Males and females of dioecious plants often differ in morphological, physiological and life‐history traits, probably as a result of their different requirements for reproduction. We found that the growth and reproductive effort of individuals of the dioecious herb Mercurialis annua depended on whether males or females had been growing in the soil previously. This suggests that males and females of M. annua differentially modify the soil in which they are growing. Our study indicates that sexual dimorphism in dioecious plants can give rise to increased environmental heterogeneity as a consequence of sex‐specific niche modification.     

Intrapopulation sex ratio variation in the salt grass Distichlis spicata

ABSTRACT In many dioecious plant populations, males and females appear to be spatially segregated, a pattern that is difficult to explain given its potentially high costs. However, in asexually propagating species, spatial segregation of the sexes may be indistinguishable from superficially similar patterns generated by random establishment of a few genets followed by extensive clonal spread and by gender-specific differences in rates of clonal spread. In populations where a significant fraction of individuals are not flowering and gender cannot be assigned to this fraction, apparent spatial segregation of the sexes may be due to differential flowering between the sexes. We confirm reports that flowering ramets of the clonal, perennial grass Distichlis spicata are spatially segregated by sex. We extend these studies in two fundamental ways and demonstrate that this species exhibits true spatial segregation of the sexes. First, using RAPD markers, we estimated that at least 50% of ramets in patches with biased sex ratios represent distinct genotypes. Second, we identified a RAPD marker linked to female phenotype (eliminating the possibility that gender is environmentally determined) and used it to show that the majority of patches exhibit significantly biased sex ratios for both ramets and genets, regardless of flowering status.     

Differential competitive ability between sexes in the dioecious Antennaria dioica (Asteraceae)

Background and Aims

Differences in competitive ability between the sexes of dioecious plants are expected as a result of allocation trade-offs associated with sex-differential reproductive costs. However, the available data on competitive ability in dioecious plants are scarce and contradictory. In this study sexual competition was evaluated using the dioecious plant Antennaria dioica in a common garden transplantation experiment.

Methods

Male and female plants were grown for 3 years either in isolation, or in competition with a plant of the same sex or the opposite sex. Flowering phenology, sexual and asexual reproduction, plant growth, nutrient content and arbuscular mycorrhizal colonization in the roots were assessed.

Key Results

Our results showed little evidence of sexual differences in competitive ability. Both sexes suffered similarly from competition, and competitive effects were manifested in some traits related to fitness but not in others. Survival was unaffected by competition, but competing plants reduced their vegetative growth and reproductive investment compared with non-competing plants. In addition, differences in sexual competitive ability were observed in relation to flowering frequency, an important life history trait not reported in previous studies.

Conclusions

The findings indicate that female and male A. dioica plants possess similar intersexual competitive abilities which may be related to the similar costs of reproduction between sexes in this species. Nevertheless, intrasexual competition is higher in females, giving support for asymmetric niche segregation between the sexes.     

No differential consequences of reproduction according to sex in Juniperus communis var. depressa (Cupressaceae)

In dioecious plant species, males and females are thought to have dissimilar allocation patterns. Females are believed to invest more in reproduction and less in growth and maintenance than males. This differential investment between sexes could result in distinct growth patterns and contrasting survival rates, thereby affecting the sex ratio of a population and the age and size distribution of males and females, possibly leading to habitat segregation according to sex. These effects might become more apparent under particularly limiting conditions, such as in nutrient-deficient soils or in climatically stressed environments. To verify these predictions, growth patterns, microsite characteristics, and age and size distribution of male and female individuals were compared, and population sex ratio was determined in three populations of the dioecious shrub Juniperus communis var. depressa (Cupressaceae, Pinophyta) along a short latitudinal gradient on the eastern coast of Hudson Bay (Northern Québec, Canada). We found that the northernmost population had a male-biased sex ratio, but that the southernmost one had a higher proportion of females. Our results failed to reveal any significant differences in radial growth patterns, mean sensitivity, annual elongation of the main axis, and size and age frequency distribution between males and females in any population. Furthermore, there was no evidence of microhabitat segregation according to sex as indicated by the lack of differences in the physicochemical characteristics of the substrate under males and females. Clearly, the expected ecological consequences of a presumed greater investment of females in reproduction were not apparent even under the very stressful conditions prevailing on subarctic dunes. Many factors could reduce differences in the cost of reproduction between males and females, such as the number and quality of reproductive structures produced annually by individuals of each sex, the possible photosynthetic activity of the immature female cones, and the complexity of the source/sink relationship within individuals. Alternatively, there may be no differences between sexes in their reproductive investment.     

Phenology, sex ratio, and spatial distribution among dioecious species of Trichilia (Meliaceae)

The flowering, sex ratio, and spatial distribution of four dioecious species of Trichilia (Meliaceae) were studied in a semi-deciduous forest in southeastern Brazil. All reproductive trees (T. clausseni, T. pallida and T. catigua) with dbh > or = 5 cm within a 1-ha plot were collected, sexed, mapped and, for individuals of each species, the distances to the nearest neighbour of the same and opposite sex were measured. For the shrub species T. elegans (dbh < 5 cm), all reproductive individuals were sampled randomly in 10 samples of 10 x 10 m. The reproductive phenology was observed at weekly to monthly intervals from May 1988 to January 1990. The species are strictly dioecious, did not present any sex-mixed trees or sex switching during the study, and sex ratio did not differ significantly from 1 : 1. The size distributions and the relative size variation were not significantly different between sexes. There was no significant segregation or clumping between individuals of either sex and no fruit production without pollination. Onset of flowering and flowering peak were synchronous between male and female plants for all species studied. Flower synchrony was related to outcrossing and pollinator attraction rather than climatic factors.     

Family affiliation,sex ratio and sporophyte frequency in unisexual mosses

Patterns of sex expression and sex ratios are key features of the life histories of organisms. Bryophytes are the only haploid‐dominant land plants. In contrast with seed plants, more than half of bryophyte species are dioecious, with rare sexual expression and sporophyte formation and a commonly female‐biased sex ratio. We asked whether variation in sex expression, sex ratio and sporophyte frequency in ten dioecious pleurocarpous wetland mosses of two different families was best explained by assuming that character states evolved: (1) in ancestors within the respective families or (2) at the species level as a response to recent habitat conditions. Lasso regression shrinkage identified relationships between family membership and sex ratio and sporophyte frequency, whereas environmental conditions were not correlated with any investigated reproductive trait. Sex ratio and sporophyte frequency were correlated with each other. Our results suggest that ancestry is more important than the current environment in explaining reproductive patterns at and above the species level in the studied wetland mosses, and that mechanisms controlling sex ratio and sporophyte frequency are phylogenetically conserved. Obviously, ancestry should be considered in the study of reproductive character state variation in plants. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 163–172.     

Local sex-ratio dynamics: a model for the dioecious liverwort Marchantia inflexa

In many dioecious bryophyte species, population sex ratios range from all female to all male. The focal species of the present study, the liverwort Marchantia inflexa, forms patches on rock and bark surfaces, and these differ widely in sex ratio at a rainforest field site in Trinidad. This analysis – to our knowledge the first modeling study of sex-ratio dynamics in a dioecious clonal organism – addresses abundances of male and female M. inflexa through time within an individual patch. We represent the life history of this species using seven different stages (non-reproductive, asexually reproductive, sexually reproductive males, non-reproductive, asexually reproductive, unfertilized and fertilized sexual females) and express their dynamics using ordinary differential equations. Some of the stages become more abundant as thalli extend over the substrate and may overgrow each other to capture space. Our simple representation of dynamics within the patch failed to stabilize the sex ratio: females gradually eliminated males at low to moderate disturbance frequency and males eliminated females at high disturbance frequency. This pattern did not hinge on whether sexual propagules could germinate within the patch, but asexual reproduction (via gemmae dispersed within the patch) played an important role. This suggests that the maintenance of sex in these populations may hinge on metapopulation structure and dynamics. Though sexual reproduction appears to be unimportant within patches, spores provide the primary means of recolonizing patches eliminated by large-scale disturbances. We found that shortly after the patch was fully occupied, the production of these wind-dispersed spores was maximized, but spore production declined thereafter as the sex ratio became increasingly biased toward one sex or the other. Much additional modeling and empirical work is needed to link within-patch dynamics across patches and account for dynamics at the metapopulation level.     

Effects of temperature and rainfall variation on population structure and sexual dimorphism across the geographical range of a dioecious species

The effects of climate (precipitation and temperature) on sexual dimorphism and population structure were analysed along a broad-scale environmental gradient covering the distributional range of the endemic dioecious species Corema album, along the west coast of the Iberian Peninsula. We aimed to assess distribution constraints and sex-related differences in demography and size associated with higher reproductive investment in females. Nine populations were chosen from across the geographic range of C. album and ten 10 × 10 m plots were established (10 m apart) along a 200-m transect. All male, female and non-reproductive shrubs were quantified within each plot and plant size, photosynthetic layer, height, sex ratio, population density and structure, and spatial segregation of sexes, under environmental conditions ranging from temperate to Mediterranean climate, were recorded and analysed. Increased aridity was related to lower population density and less structured populations, indicating an effect of higher temperature and lower precipitation on regeneration. Sexual dimorphism was influenced by climate, with size differences between sexes varying with aridity. However, demographic differences between sexes reflected in sex ratio deviations or the occurrence of spatial segregation were unrelated to any climatic variable, suggesting the existence of compensatory mechanisms that may counterbalance the higher reproductive effort of female plants. The results show the vulnerability of this endemic species to the increase in aridity expected in the southernmost limit of the biogeographical area due to global climate change, and demonstrate the importance of broad scale studies in the assessment of sexual dimorphism.     

Sexual dimorphism,temporal niche differentiation,and evidence for the Jack Sprat effect in an annual dioecious plant

Sexual dimorphism in dioecious plants often occurs as a consequence of the different resource requirements of females and males, especially during reproduction. The contrasting reproductive roles of the sexes can influence the phenology of growth, plant size, and flowering time, with implications for the intensity of competitive interactions within and between the sexes. Here, we investigate the influence of contrasting nutrient regimes and intra-sexual and inter-sexual competition on the expression of sexual dimorphism in life-history traits and biomass allocation throughout the life cycle of the dioecious annual Rumex hastatulus Baldw. (Polygonaceae). Development of a sex-specific marker enabled us to quantify the influence of competition on sex-specific differences in mortality and vegetative traits. We were particularly interested in determining whether the overall performance of the sexes might differ between the two forms of intra-specific competition, potentially providing evidence for sexual specialization in resource acquisition and niche differentiation. Our results indicated that although patterns of sexual dimorphism were dynamic, they were largely insensitive to nutrient conditions. We found that intra-sexual competition was more severe than inter-sexual competition, differentially affecting mortality and most traits during the vegetative and particularly the reproductive stage of the life history. Female trait values generally increased more under inter-sexual than intra-sexual competition in comparison to males. Our findings are consistent with temporal niche differentiation resulting from sexual specialization for different resource requirements and provide evidence for the “Jack Sprat effect.”     

Biased sex ratios in the dioecious annual Croton texensis (Euphorbiaceae) are not due to environmental sex determination

At Arapaho Prairie, in the sandhills of western Nebraska, the dioecious annual Croton texensis (Euphorbiaceae) exhibits biased sex ratios. Moreover, the direction of bias changes from year to year: in 1994 the study population was significantly female biased, in 1995 and 1996 it was significantly male biased, and in 1997 and 1998 the sex ratio did not differ from 1 : 1. Such variation in the observed sex ratio in plants is frequently attributed to environmental sex determination (ESD), which is favored by natural selection if the rate of fitness gain across an environmental gradient is greater for one sex than the other. We performed experiments to determine: (1) whether variation in the sex ratio is correlated with environmental conditions, as would be expected if ESD is operating, and (2) whether ESD, if present, would be favored by natural selection. In a common garden experiment in which water and fertilizer were manipulated the sex ratio was marginally male biased in treatments in which water was added, but not different from 1 : 1 in other treatments. In field plots into which seeds were planted none of several soil characteristics, nor overall plot quality for C. texensis (measured as average plant biomass) were correlated with plot sex ratio. However, plots in which a large number of planted seeds emerged tended to be female biased. These results provide very weak evidence for sex ratio bias across an environmental gradient, and thus provide little evidence for ESD. Moreover, sex-by-environment interactions for fitness, which are required for the evolution of ESD, were absent for all measured variables. Thus, ESD does not appear to be favored by natural selection in this population. Instead, these biases may have been caused by differences between the sexes in germination and/or early mortality.