Allometry of sexual size dimorphism in dioecious plants: do plants obey Rensch's rule?

Rensch's rule refers to a pattern in sexual size dimorphism (SSD) in which SSD decreases with body size when females are the larger sex and increases with body size when males are the larger sex. Many animal taxa conform to Rensch's rule, but it has yet to be investigated in plants. Using herbarium collections from New Zealand, we characterized the size of leaves and stems of 297 individuals from 38 dioecious plant species belonging to three distantly related phylogenetic lineages. Statistical comparisons of leaf sizes between males and females showed evidence for Rensch's rule in two of the three lineages, indicating SSD decreases with leaf size when females produce larger leaves and increases with leaf size when males produce larger leaves. A similar pattern in SSD was observed for stem sizes. However, in this instance, females of small-stemmed species produced much larger stems than did males, but as stem sizes increased, SSD often disappeared. We hypothesize that sexual dimorphism in stem sizes results from selection for larger stems in females, which must provide mechanical support for seeds, fruits, and dispersal vectors, and that scaling relationships in leaf sizes result from correlated evolution with stem sizes. The overall results suggest that selection for larger female stem sizes to support the weight of offspring can give rise to Rensch's rule in dioecious plants.     

Genetic correlations with floral display lead to sexual dimorphism in the cost of reproduction

In dioecious plants, females typically invest more biomass in reproduction than males and consequently experience stronger life-history trade-offs. Sexual dimorphism in life history runs counter to this pattern in Silene latifolia: females acquire less carbon and invest more biomass in reproduction, but males pay a higher cost of reproduction. The species is sexually dimorphic for many traits, especially flower number, with males producing many, small flowers compared to females. We tested whether the cost of reproduction is higher in males because flower number, which we presume to be under sexual selection in males, is genetically correlated with traits that would affect life-history trade-offs. We performed artificial selection to reduce the sexual dimorphism in flower size and looked at correlated responses in ecophysiological traits. We found significant correlated responses in total vegetative mass, leaf mass, leaf thickness, and measures of CO(2) exchange. Individuals in the many-and-small-flowered selection lines did not grow as large or invest as much biomass in leaves, and their leaves exhibited an up-regulated physiology that shortened leaf life span. Our results are consistent with the hypothesis that genetic correlations between floral display and ecophysiological traits lead to a higher cost of reproduction for males.     

蝘蜓头、体大小的两性异形和雌体繁殖

报道了蜓 (Sphenomorphusindicus)头、体大小的两性异形和雌性繁殖。性成熟雌体大于雄体。雄性成体头长大于雌性成体 ,但头宽与雌性成体无显著差异。初生幼仔的头长和头宽无两性差异。雄性幼体头长和头宽大于雌性幼体。设置SVL恒定时 ,雄性幼体和雄性成体的头长和头宽无显著差异 ,雌性幼体的头长和头宽大于雌性成体。初生幼仔具有相对较大的头部。产仔雌体的最小SVL为 6 7 7mm ,大于此SVL的雌体均年产单窝仔。平均窝仔数、窝仔重和幼仔重分别为 7 2 ( 3～ 11)、 3 34( 1 30～ 5 19)和 0 48( 0 36～ 0 5 8)g。用卵黄沉积卵巢卵和输卵管计数的窝仔数比用幼仔计数的窝仔数多约 1 0个后代。幼仔体重与雌体SVL无关。相对窝仔重与雌体SVL边缘性地呈正相关。窝仔数、窝仔重与雌体SVL呈正相关 ,幼仔体重与窝仔数呈负相关。窝仔数与雌体状态无关。     

Sex-specific pattern of spatial genetic structure in dioecious and clonal tree species, <Emphasis Type="Italic">Populus alba</Emphasis> L.

Fine-scale spatial genetic structure (SGS) has profound ecological and genetic consequences for plant populations, and some studies indicate that clonal reproduction may significantly enhance SGS. Clonality is widespread among dioecious species, but little is known about the relationship between clonal reproduction and SGS in the frame of sexual dimorphism. We asked the following questions: (1) Is there a sexually dependent pattern of SGS in white poplar population? (2) What is the relationship between clonal reproduction and SGS? and (3) Does this relationship have a sex-specific component? Using 16 microsatellite markers, genetic structure including fine-scale SGS and clonality of females and males of white poplar were investigated. Significant SGS was noted for both sexes at the ramet and genet levels. At the genet level, males had 2.7-fold higher SGS than that of females. Clonality significantly contributed to SGS only in females. A sibship structure revealed with pedigree analysis and clustering-based methods among males was likely the major factor of the observed SGS. The sexes differed in their clonal growth strategies. Spatial positioning of ramets in female clones suggested foraging behavior and/or avoidance of competition, while for male clones it indicated more expansion and space colonization. The obtained results led us to conclude that sexual dimorphism in life history traits may affect the course and rate of demo-genetic processes acting in natural populations of dioecious species. To our knowledge, this is the first study demonstrating a sex-specific pattern of SGS in natural populations of dioecious species.     

Roots, shoots and reproduction: sexual dimorphism in size and costs of reproductive allocation in an annual herb

Females tend to be smaller than males in woody dioecious plant species, but they tend to be larger in herbs. The smaller size of females in woody species has been attributed to higher reproductive costs, yet no satisfactory explanation has been provided for their larger size in herbs. Because herbs have higher nitrogen concentrations in their tissues than woody plants, and because pollen is particularly rich in nitrogen, we predicted that male growth would be more compromised by reproduction than female growth. To test this hypothesis, we conducted three experiments on the annual dioecious herb Mercurialis annua. First, we compared the timing of reproduction between males and females and found that males started flowering earlier than females; early flowering is expected to compromise growth more than later flowering. Second, we compared plants allowed to flower with those prevented from flowering by experimental debudding and found that males incurred a higher reproductive cost than females in terms of both biomass and, particularly, nitrogen. Third, we grew plants under varying levels of nitrogen availability and found that although sexual size dimorphism was unaffected by nitrogen, females, but not males, decreased their relative allocation to both roots and reproduction under high nitrogen availability. We propose that males deal with the high cost of pollen production in terms of nitrogen by allocating biomass to nitrogen-harvesting roots, whereas females pay for carbon-rich seeds and fruits by investing in photosynthetic organs. Sexual dimorphism would thus seem to be the outcome of allocation to above- versus below-ground sinks that supply resources (carbon versus nitrogen) limiting the female and male reproduction differentially.     

Causes of secondary sexual differences in plants — Evidence from extreme leaf dimorphism in Leucadendron (Proteaceae)

In extreme cases leaves in male plants of the dioecious genus Leucadendron (Proteaceae) are up to an order of magnitude smaller than female leaves. This secondary sexual dimorphism (SSD) in leaf size has previously been suggested to be due to intra-male sexual selection, leading to an increase in male allocation to reproduction in dimorphic species. After critically evaluating previous data provided to support this hypothesis, I suggest on both theoretical grounds and on re-analysis that this argument is unlikely and unsupported. Leaf size dimorphism could theoretically evolve directly due to disruptive ecological selection between genders, leading to niche dimorphism either within or between habitats. I test this ecological causation hypothesis by providing data on specific leaf area (sla) and water use efficiency (δ ¹³C) of leaves from males and females of several Leucadendron species. Results confirm the expectation of minimal gender differences. I argue that leaf dimorphism is a consequence of selection on flower size and architecture.     

Sexual dimorphism and seasonal changes of leaf gas exchange in the dioecious tree Ilex paraguariensis grown in two contrasted cultivation types

Yerba maté (Ilex paraguariensis, Aquifoliaceae) is a subtropical, evergreen, dioecious, South American tree. In one preliminary study, it was observed that the functional strategy of yerba mate females, aiming to finish reproductive process, was increased transpiration relative to photosynthetic rates compared with males, on self‐shaded leaves. We hypothesised that the long‐term gas exchange response of males and females can evolve independently of phenological stage and cultivation type. In this spirit, the primary aim of the study was to analyse the physiological sexual dimorphism of this species, evaluating fluctuations of gas exchanges related to microclimate and phenological stages. A field study was conducted on adult plants of yerba maté cultivated in monoculture (MO) and in forest understorey (FUS), and measurements carried out in situ on microclimate and leaf gas exchange parameters. The photosynthetic photon flux density that was attained at leaf level in FUS was reduced roughly 10‐fold compared with that in MO. Various leaf age populations were observed during a 2‐year period at 2‐month intervals and grouped into four categories: young, young‐fully‐expanded, fully‐expanded and old. Young and young‐fully‐expanded leaves were the most active in photosynthesis. Leaves of female plants showed greater photosynthetic rate than those of male plants, which was expressed on all leaf age categories in MO, but only during vegetative stages previous to flowering and fruit ripening. The photosynthesis of young‐fully‐expanded leaves of females grown in FUS was superior to males but only during winter growth pause. The stomatal conductance differed in relation to cultivation type and leaf age but did not show the sexual differentiation. Physiological sexual dimorphism in yerba mate is shown to be plastic, responding to environmental conditions. The cost associated to the reproduction of yerba maté could be most easily met showing physiological differentiation of both sexes. A higher reproductive investment of females might be compensated for by exhibiting greater leaf photosynthesis than males that occurs in vegetative stages that precede flowering and fruit ripening.     

Genetic differences among populations in sexual dimorphism: evidence for selection on males in a dioecious plant

Genetic variation among populations in the degree of sexual dimorphism may be a consequence of selection on one or both sexes. We analysed genetic parameters from crosses involving three populations of the dioecious plant Silene latifolia, which exhibits sexual dimorphism in flower size, to determine whether population differentiation was a result of selection on one or both sexes. We took the novel approach of comparing the ratio of population differentiation of a quantitative trait (Q(ST) ) to that of neutral genetic markers (F(ST) ) for males vs. females. We attributed 72.6% of calyx width variation in males to differences among populations vs. only 6.9% in females. The Q(ST) /F(ST) ratio was 4.2 for males vs. 0.4 for females, suggesting that selection on males is responsible for differentiation among populations in calyx width and its degree of sexual dimorphism. This selection may be indirect via genetic correlations with other morphological and physiological traits.     

Patterns of growth and sexual size dimorphism in two species of box turtles with environmental sex determination

An adaptive explanation for environmental sex determination is that it promotes sexual size dimorphism when larger size benefits one sex more than the other. That is, if growth rates are determined by environment during development, then it is beneficial to match developmental environment to the sex that benefits more from larger size. However, larger size may also be a consequence of larger size at hatching or growing for a longer time, i.e., delayed age at first reproduction. Therefore, the adaptive significance of sexual size dimorphism and environmental sex determination can only be interpreted within the context of both growth and maturation. In addition, in those animals that continue to grow after maturation, sexual size dimorphism at age of first reproduction could differ from sexual size dimorphism at later ages as growth competes for energy with reproduction and maintenance. I compared growth using annuli on carapace scales in two species of box turtles (Terrapene carolina and T. ornata) that have similar patterns of environmental sex determination but, reportedly, have different patterns of sexual size dimorphism. In the populations I studied, sexual size dimorphism was in the same direction in both species; adult females were, on average, larger than adult males. This was due in part to males maturing earlier and therefore at smaller sizes than females. In spite of similar patterns of environmental sex determination, patterns of growth differed between the species. In T. carolina, males grew faster than females as juveniles but females had the larger asymptotic size. In T. ornata, males and females grew at similar rates and had similar asymptotic sizes. Sexual size dimorphism was greatest at maturation because, although males matured younger and smaller, they grew more as adults. There was, therefore, no consistent pattern of faster growth for females that may be ascribed to developmental temperature. Received: 20 March 1996 / Accepted: 10 March 1998     

Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae)>

We examined sexual dimorphism in reproductive allocation and its effects on growth and subsequent reproduction in a natural population of the dioecious woody shrub Lindera benzoin (L.) Blume. In addition to comparing natural patterns of growth and reproduction in a marked population of 251 females and 87 males, we experimentally examined the effect of reduced reproduction on future growth and reproduction in female plants and examined sexual dimorphism in carbon/nutrient balance. Our results suggest that females of L. benzoin bear greater reproductive costs in terms of both biomass and minerals. These costs were measurable in terms of current biomass and allocation of nitrogen to reproduction, as well as subsequent growth, reproduction, and tissue carbon/nutrient balance. Based upon the results of a fruit-thinning experiment and path analysis, fruit production in 1991 appeared to have direct negative effects on fruit production in 1992, an effect that was not necessarily mediated through effects on plant growth. We discuss our results in the context of other intrinsic and extrinsic factors that can influence growth, reproductive costs, and mortality in this species.     

Costs of reproduction in Nyssa sylvatica: sexual dimorphism in reproductive frequency and nutrient flux

Summary We examined the influence of differential reproductive frequency between the sexes on tertiary (phenotypic) sex ratios in the the dioecious tree Nyssa sylvatica (Nyssaceae). Reproduction was evaluated in relation to sex, size and canopy exposure using flowering data collected from 1229 marked trees over a four year period. For subsets of each population we used data on flower number, fruit crop size, fruit/flower ratios, and individual flower and fruit mass to compare biomass invested in reproductive structures of males and females. We also examined seasonal changes in stem nitrogen and soluble carbohydrate content in relation to flower and fruit production for trees of each sex. Our results indicate that: 1) Male-biased tertiary sex ratios could be explained by more frequent reproduction by male trees; 2) Estimated secondary sex ratios based on sums of all known males and females were not significantly different from 1:1; 3) Flowering frequency of males and females was significantly related to plant size (DBH) and exposure of the canopy to light; 4) Estimtes of reproductive biomass allocation ranged from 1.36 to 10.8 times greater for females relative to males; 5) Flower production was related to stem nutrient status for both sexes, but nutrient depletion and its effect on subsequent flowering was much more pronounced for female trees. We conclude that less frequent flowering by female trees may result from depletion of stored reserves, and that differential flowering frequency in N. sylvatica may ultimately reduce apparent sexual differences in the costs of reproduction.     

Structural and physiological sexual dimorphism estimated from three‐dimensional virtual trees of yerba‐mate (Ilex paraguariensis) is modified by cultivation environment

Yerba‐mate is a subtropical, evergreen, dioecious, South American tree. Sexual dimorphism in photosynthesis, leaf allometry and foliage distribution was hypothesised. Virtual trees (constructed in VPlants software from detailed measurements of plant morphogenesis) of the two genders were compared considering two contrasted cultivation environments and three developmental stages. The total crown volume, leaf area per plant (LA), leaf area index (LAI) and leaf area density (LAD) were calculated. The light interception and photosynthesis were computed from mock‐ups in VegeSTAR. Structural sexual dimorphism concerned general plant form, internode length, leaf allometry, leaf surface, pattern of leaf area distribution and LAD. Cultivation environment and developmental stage acted strongly on sex expression of all observed structural parameters and physiological stages. Sexual differentiation in LA and light interception was related to leaves positioned in the lowest layers (150 cm above ground), whereas sexual specialisation in leaf and plant photosynthesis was related to early vegetative and reproductive stages. Several sexual responses strongly depended on the environment, especially light conditions, with opposite effects observed on female and male plants whether they were cultivated in monoculture or in forest understorey, under high‐light condition or low‐light condition, respectively. Optimised foliage structure and physiology in females may compensate for greater reproductive costs in early developmental stages, but females and males equalise in photosynthetic efficiency after 2‐year regrowth.     

Reproduction, development and growth of Akodon lindberghi (Hershkovitz, 1990) (Rodentia, Muridae, Sigmodontinae) raised in captivity

The reproduction, development and growth of Akodon lindberghi were studied in captivity. The colony was derived from animals captured in Sim?o Pereira, Minas Gerais state, which represents a new area of geographical distribution known for this species. Twelve males and twelve females were crossed, producing 144 young in 53 litters. Post-partum oestrus was observed and gestation length was estimated in 23 days. Litter size ranged from 1 to 4 with a mean of 2.72 (SD = 0.97, n = 53) and modal size of 3. Sexual dimorphism was neither present in body mass at birth nor at weaning. There was a significant negative correlation between litter size and mass at birth or weaning. Permanent emergence of adult external appearance occurred at 15 days. Puberty for males and females was 43 and 42 days, respectively, and the first fecundation event for two females was recorded at 47 and 54 days of age. The weight growth was described by fitting a Gompertz model. No significant difference was found in any parameter of growth curves for males and females. Measurements (head-body, tail, hind foot and internal and external ear lengths) obtained for adult individuals also did not reveal the presence of sexual dimorphism.     

Sexual and vegetative reproduction in the aboveground part of a dioecious clonal plant, <Emphasis Type="Italic">Dioscorea japonica</Emphasis> (Dioscoreaceae)

In dioecious clonal plants, the reproductive effort required to set seeds will be responsible for the larger investment in sexual reproduction by females. If there will be a trade-off in resource allocation between sexual and clonal reproduction, this differential sexual reproduction will lead to sexual differentiation in the relative amount of clonal reproduction. To test this prediction, we studied differences between the sexes in their phenologies and investments in sexual and vegetative reproduction (clonal reproduction by means of bulbils) with respect to ramet size in a dioecious clonal plant, Dioscorea japonica Thunb. The period of bulbil production overlapped the period during which infructescences developed. Females flowered later, produced heavier inflorescences, and fewer flowers per inflorescence than did males. Regression analysis using the size of the individual plants demonstrated that large females made smaller investments in inflorescences and larger investments in sexual reproduction than did large males. In contrast, females invested fewer resources in vegetative reproduction than did males. However, the total investments in sexual and vegetative reproduction did not differ between the sexes. These results supported our hypothesis on the sexual differentiation in sexual and clonal reproduction.     

Pollinator responses to variation in floral display and flower size in dioecious Sagittaria latifolia (Alismataceae)

In animal-pollinated plants with unisexual flowers, sexual dimorphism in floral traits may be the consequence of pollinator-mediated selection. Experimental investigations of the effects of variation in flower size and floral display on pollinator visitation can provide insights into the evolution of floral dimorphism in dioecious plants. Here, we investigated pollinator responses to experimental arrays of dioecious Sagittaria latifolia in which we manipulated floral display and flower size. We also examined whether there were changes in pollinator visitation with increasing dimorphism in flower size. In S. latifolia, males have larger flowers and smaller floral displays than females. Visitation by pollinators, mainly flies and bees, was more frequent for male than for female inflorescences and increased with increasing flower size, regardless of sex. The number of insect visits per flower decreased with increasing floral display in males but remained constant in females. Greater sexual dimorphism in flower size increased visits to male inflorescences but had no influence on the number of visits to female inflorescences. These results suggest that larger flower sizes would be advantageous to both females and males, and no evidence was found that females suffer from increased flower-size dimorphism. Small daily floral displays may benefit males by allowing extended flowering periods and greater opportunities for effective pollen dispersal.     

Similar gender dimorphism in the costs of reproduction across the geographic range of Fraxinus ornus

BACKGROUND AND AIMS: The reproductive costs for individuals with the female function have been hypothesized to be greater than for those with the male function because the allocation unit per female flower is very high due to the necessity to nurture the embryos until seed dispersal occurs, while the male reproductive allocation per flower is lower because it finishes once pollen is shed. Consequently, males may invest more resources in growth than females. This prediction was tested across a wide geographical range in a tree with a dimorphic breeding system (Fraxinus ornus) consisting of males and hermaphrodites functioning as females. The contrasting ecological conditions found across the geographical range allowed the evaluation of the hypothesis that the reproductive costs of sexual dimorphism varies with environmental stressors. METHODS: By using random-effects meta-analysis, the differences in the reproductive and vegetative investment of male and hermaphrodite trees of F. ornus were analysed in 10 populations from the northern (Slovakia), south-eastern (Greece) and south-western (Spain) limits of its European distribution. The variation in gender-dimorphism with environmental stress was analysed by running a meta-regression between these effect sizes and the two environmental stress indicators: one related to temperature (the frost-free period) and another related to water availability (moisture deficit). KEY RESULTS: Most of the effect sizes showed that males produced more flowers and grew more quickly than hermaphrodites. Gender differences in reproduction and growth were not minimized or maximized under adverse climatic conditions such as short frost-free periods or severe aridity. CONCLUSIONS: The lower costs of reproduction for F. ornus males allow them to grow more quickly than hermaphrodites, although such differences in sex-specific reproductive costs are not magnified under stressful conditions.     

Sexual selection,sexual dimorphism and plant phylogeny

Summary Darwin examined sexual dimorphism in animals, arguing that sexual selection was important in the evolution of such dimorphism. Sexual dimorphism in plants may have parallel causes and costs.The processes that contribute to sexual dimorphism may also lead to speciation and morphological differences among related species, as argued originally by Darwin. Where sexes are separate and dimorphism is well-developed, males of related animal species (both vertebrate and invertebrate) are often strikingly different from each other, while females may be virtually indistinguishable. A similar pattern may exist in plants: it is frequently the males (of dioecious taxa) or the male portions of the flower (in co-sexual flowers) that apparently have diversified. I suggest that the similarity of pattern may be accounted for by a similarity of process.In addition, sexual selection may have contributed to certain evolutionary trends within the angiosperms and, indeed, to angiosperm radiation.     

Sex and Weapons: Contrasting Sexual Dimorphisms in Weaponry and Aggression in Snapping Shrimp

Sexual dimorphisms in weaponry and aggression are common in species in which one sex (usually males) competes for access to mates or resources necessary for reproduction – sexually dimorphic weaponry and aggression, in other words, are frequently the result of intrasexual selection. In snapping shrimp, the major chela (snapping claw) can be a deadly weapon, and males of many species have larger chelae than females, a pattern readily interpreted as resulting from intrasexual selection. Thus, males might be expected to show more sex‐specific aggression than females, and be more aggressive overall. We tested these predictions in two species of snapping shrimp in a territorial defense context. Neither of these predictions was supported: in both species, females, but not males, engaged in sex‐specific aggression and females were more aggressive than males overall. These contrasting sexual dimorphisms – larger weaponry in males but higher aggression in females – highlight the importance of considering the function of weaponry and aggression in contexts other than direct competitions over mates. In addition, species differences in the degree of sexual dimorphism in chela size were due to differences in female, not male, chela size, and the species with greater sexual dimorphism in weaponry was significantly less aggressive overall; also, while paired and solitary males did not differ in residual chela size, for the species with greater sexual dimorphism, females carrying embryos had smaller residual chela sizes. These results suggest that understanding the sexual dimorphisms in weaponry and aggression in snapping shrimp requires understanding the relative costs and benefits of both in females as well as males.     

Flying the nest: male dispersal and multiple paternity enables extrafamilial matings for the invasive bark beetle Dendroctonus micans

There is an evolutionary trade-off between the resources that a species invests in dispersal versus those invested in reproduction. For many insects, reproductive success in patchily-distributed species can be improved by sibling-mating. In many cases, such strategies correspond to sexual dimorphism, with males–whose reproductive activities can take place without dispersal–investing less energy in development of dispersive resources such as large body size and wings. This dimorphism is particularly likely when males have little or no chance of mating outside their place of birth, such as when sperm competition precludes successful fertilisation in females that have already mated. The economically important bark beetle pest species Dendroctonus micans (Coleoptera: Curculionidae, Scolytinae) has been considered to be exclusively sibling-mating, with 90% of females having already mated with their brothers by emergence. The species does not, however, show strong sexual dimorphism; males closely resemble females, and have been observed flying through forests. We hypothesised that this lack of sexual dimorphism indicates that male D. micans are able to mate with unrelated females, and to sire some or all of their offspring, permitting extrafamilial reproduction. Using novel microsatellite markers, we carried out cross-breeding laboratory experiments and conducted paternity analyses of resulting offspring. Our results demonstrate that a second mating with a less-related male can indeed lead to some offspring being sired by the latecomer, but that most are sired by the first, sibling male. We discuss these findings in the context of sperm competition versus possible outbreeding depression.     

Sex ratio variation in dioecious plant species: A comparative ecological study of six species of Lindera (Lauraceae)

Sex ratio variation was investigated in natural populations of six dioecious shrub species of Lindera in Japan. Interspecific differences in sex ratio were examined in relation to patterns of population structure, floral dimorphism, fruit production and intersexual differences in herbivory. Sex ratios tended towards equality or bias in favour of males, except for populations of L. glauca , in which no male plants were found. Sex switching in individual plants was not observed. Although male flowers were generally larger in size than flowers of conspecific females, costs of flowering did not appear to influence sex ratio. However, a relation was found between high allocation to fruit production and increasing male fraction of populations. In addition, girths of flowering plants tended to be larger in females, which may indicate delay in age of the first reproduction compared to males. No intersexual difference was found in degree of leaf damage due to herbivory. Results of this study are discussed in the light of other studies on sex ratio variation in dioecious plant species.