Sexual dimorphism in clonal growth forms and ramet distribution patterns in <Emphasis Type="Italic">Rumex acetosella</Emphasis> (Polygonaceae)

We investigated clonal traits in the dioecious herb Rumex acetosella to characterize sexual dimorphism in clonal forms and to correlate below-ground clonal patterns and above-ground ramet distributions. We recorded creeping root length, branching patterns, ramet and clump (caespitose ramets from the same position on the root) sprouting patterns, and biomass allocations in three females and males. We also estimated the patch size of flowering ramets within a quadrat. No sexual dimorphism was detected in the frequencies of branches and flowering ramets per root length. Male plants allocated proportionally more biomass to below-ground organs. Total root length did not differ between the sexes. Females sprouted more clumps with fewer flowering ramets per root length than males, which sprouted fewer clumps with more flowering ramets, which meant that clump sprouting patterns were phalanx-like in females and guerrilla-like in males. Flowering ramets were aggregately distributed in both females and males and patch sizes were similar between sexes, indicating that the spreader propagations were not found in the guerrilla-like males. We assumed that sexual dimorphism occurred in response to physiological integration for higher reproductive effort in females.     

Sexual dimorphism and sex ratios of two Australian dioecious species of alpine pineapple grass, Astelia alpina var. novaehollandiae and Astelia psychrocharis (Asteliaceae)

Sexual dimorphism and male biased sex ratios have been predicted for dioecious plants experiencing the limited conditions for growth and reproduction found in many alpine environments. To test these predictions, the reproductive ecology of two congeneric, co-occurring, dioecious, clonal, species was examined in the subalpine and alpine zones of Kosciuszko National Park, southeastern Australia. Specifically, plant size (vegetative cover of plants in quadrats), floral display (number of flowers per inflorescence, number of inflorescences per quadrat) and sex ratios (proportion of females in quadrats with flowers) were examined in ten populations of Astelia psychrocharis (Asteliaceae) and nine populations of Astelia alpina var. novae-hollandiae (Asteliaceae). Sexual dimorphism did occur, with males having more flowers per inflorescence (106% more flowers for A.alpina males and 12% more for A.psychrocharis males compared to females) and more inflorescences per quadrat than females (78% more inflorescences for A.alpina males and 46% more inflorescences for A.psychrocharis males compared to females). Plant size did not differ between male and female quadrats of either species, nor were there male biased sex ratios. However, plant size was related to flowering status in A.psychrocharis with the 65 quadrats that did not flower having lower vegetative cover than the 175 flowering quadrats indicating that there may be a minimum size/ cover required prior to flowering in this species. For A.alpina, all but two of the 185 quadrats randomly sampled flowered. There was no effect of altitude on plant size and very little effect of altitude on floral display for either species, apart from a slight increase in the number of inflorescences per quadrat with increasing altitude for A.psychrocharis, and slight decrease in number of flowers per inflorescence with increasing altitude for A.alpina females.     

Flower bud abortion influences clonal growth and sexual dimorphism in the understorey dioecious shrub Aucuba japonica (Cornaceae)

Sexual differences were investigated to determine the significance of flower bud abortion in the dioecious shrub Aucuba japonica Thunb. The mean number of flowers per inflorescence and the mean number of flowering inflorescences (as opposed to aborted inflorescences) per individual were greater in males than in females in 1997 and 1998. Reproductive investment by males was 0.4-times (1997) and 1.4-times (1998) that by females. In addition, females aborted 30.9% (1997) and 42.7% (1998) of their total flower buds without blooming, whereas no male flower buds aborted. One of the architectural traits of this shrub is that in the year that a flower bud is produced at the shoot apex, the shoot will branch into two or more shoots. Thus, there was less sexual difference in the number of current shoots per individual than there was in the number of flowering inflorescences. The relationship between annual growth and reproduction, and the probability of reproduction in the following year, suggested that the higher investment in female reproduction was manifested as a cost for reproductive frequency rather than as a cost for annual growth. The spatial distribution of both males and females was clumped, which may be the result of clonal growth. In addition, overall sex ratios were not skewed and the number of sprouts did not differ significantly between sexes. These results suggested that flower bud abortion by females might reduce sexual dimorphism in terms of clonal growth.     

Life‐history trade‐offs promote the evolution of dioecy

Most dioecious plants are perennial and subject to trade‐offs between sexual reproduction and vegetative performance. However, these broader life‐history trade‐offs have not usually been incorporated into theoretical analyses of the evolution of separate sexes. One such analysis has indicated that hermaphroditism is favoured over unisexuality when female and male sex functions involve the allocation of nonoverlapping types of resources to each sex function (e.g. allocations of carbon to female function vs. allocations of nitrogen to male function). However, some dioecious plants appear to conform to this pattern of resource allocation, with different resource types allocated to female vs. male sex functions. Using an evolutionarily stable strategy approach, we show that life‐history trade‐offs between sexual reproduction and vegetative performance enable the evolution of unisexual phenotypes even when there are no direct resource‐based trade‐offs between female and male sex functions. This result might help explain the preponderance of perennial life histories among dioecious plants and why many dioecious plants with annual life histories have indeterminate growth with ongoing trade‐offs between sexual reproduction and vegetative growth.     

SEXUAL DIMORPHISM IN BIOMASS ALLOCATION AND CLONAL GROWTH OF XANTHOXYLUM AMERICANUM

Reproduction can have a high resource cost. It has been suggested that greater investments in sexual reproduction by female dioecious plants leads to a lower rate of vegetative growth in females than in males. In this study, we investigated sexual dimorphism in biomass allocation and genet growth of the dioecious clonal shrub, northern prickly ash (Xanthoxylum americanum). The allocation of biomass over the course of one growing season to reproductive tissue, leaves, and growth of aboveground first-year wood, was compared in 18 clones growing in fields and six clones in woods in southeastern Wisconsin during 1985 and 1986. In addition, the number of shoots per clone, and weight of nonfirst-year wood (accumulated biomass) above- and below-ground were estimated. In open field sites, male clones allocated more biomass to new wood and less to reproduction than females, although males allocated more to flowers alone. Accordingly, male clones had significantly more shoots and more accumulated biomass both above- and below-ground than female clones. In the woods, where fruit set was near zero, there were few significant differences between male and female clones in either biomass allocation or accumulated biomass. These results support the hypothesis that the high resource investment in fruit production by females reduces their vegetative growth relative to males.     

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.”     

Costs of reproduction as related to the timing of phenological phases in the dioecious Shrub Pistacia lentiscus L

Females of woody dioecious species usually devote more resources to reproduction than males. This may lead to a decrease in female survival and growth. The costs of reproduction, however, can be lightened through a number of mechanisms, as for example avoiding the temporal coincidence of reproduction and vegetative growth. The aim of this study was to evaluate whether males and females of P. lentiscus differ in the timing of their vegetative growth, and to assess whether the sequencing of vegetative growth and reproduction reduces reproductive costs. We monitored phenology in males and females. We also compared male and female allocation of nutrients and biomass in the branch, and the developmental stability of the growing shoots. We did this both prior to and at the end of the fruiting period. Males and females showed similar vegetative and flowering phenologies. Males invested more biomass in flowering, but the sexes showed equal vegetative biomass and nutrient content prior to the fruiting period. In female branches, no trade-off was found between fruit load and current-year vegetative growth. In P. lentiscus, avoiding the overlap of flowering, vegetative growth and fruiting probably contributes to reduce the immediate costs of reproductive efforts, both in males and females.     

Does the silver moss Bryum argenteum exhibit sex-specific patterns in vegetative growth rate,asexual fitness or prezygotic reproductive investment?

Background and Aims

Expected life history trade-offs associated with sex differences in reproductive investment are often undetected in seed plants, with the difficulty arising from logistical issues of conducting controlled experiments. By controlling genotype, age and resource status of individuals, a bryophyte was assessed for sex-specific and location-specific patterns of vegetative, asexual and sexual growth/reproduction across a regional scale.

Methods

Twelve genotypes (six male, six female) of the dioecious bryophyte Bryum argenteum were subcultured to remove environmental effects, regenerated asexually to replicate each genotype 16 times, and grown over a period of 92 d. Plants were assessed for growth rates, asexual and sexual reproductive traits, and allocation to above- and below-ground regenerative biomass.

Key Results

The degree of sexual versus asexual reproductive investment appears to be under genetic control, with three distinct ecotypes found in this study. Protonemal growth rate was positively correlated with asexual reproduction and sexual reproduction, whereas asexual reproduction was negatively correlated (appeared to trade-off) with vegetative growth (shoot production). No sex-specific trade-offs were detected. Female sex-expressing shoots were longer than males, but the sexes did not differ in growth traits, asexual traits, sexual induction times, or above- and below-ground biomass. Males, however, had much higher rates of inflorescence production than females, which translated into a significantly higher (24x) prezygotic investment for males relative to females.

Conclusions

Evidence for three distinct ecotypes is presented for a bryophyte based on regeneration traits. Prior to zygote production, the sexes of this bryophyte did not differ in vegetative growth traits but significantly differed in reproductive investment, with the latter differences potentially implicated in the strongly biased female sex ratio. The disparity between males and females for prezygotic reproductive investment is the highest known for bryophytes.     

Sexual dimorphism in resource acquisition and deployment: both size and timing matter

Background and Aims

The males and females of many dioecious plant species differ from one another in important life-history traits, such as their size. If male and female reproductive functions draw on different resources, for example, one should expect males and females to display different allocation strategies as they grow. Importantly, these strategies may differ not only between the two sexes, but also between plants of different age and therefore size. Results are presented from an experiment that asks whether males and females of Mercurialis annua, an annual plant with indeterminate growth, differ over time in their allocation of two potentially limiting resources (carbon and nitrogen) to vegetative (below- and above-ground) and reproductive tissues.

Methods

Comparisons were made of the temporal patterns of biomass allocation to shoots, roots and reproduction and the nitrogen content in the leaves between the sexes of M. annua by harvesting plants of each sex after growth over different periods of time.

Key Results and Conclusions

Males and females differed in their temporal patterns of allocation. Males allocated more to reproduction than females at early stages, but this trend was reversed at later stages. Importantly, males allocated proportionally more of their biomass towards roots at later stages, but the roots of females were larger in absolute terms. The study points to the important role played by both the timing of resource deployment and the relative versus absolute sizes of the sinks and sources in sexual dimorphism of an annual plant.     

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.     

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.     

Clonal genetic structure and diversity in populations of an aquatic plant with combined vs. separate sexes

Clonality is often implicated in models of the evolution of dioecy, but few studies have explicitly compared clonal structure between plant sexual systems, or between the sexes in dioecious populations. Here, we exploit the occurrence of monoecy and dioecy in clonal Sagittaria latifola (Alismataceae) to evaluate two main hypotheses: (i) clone sizes are smaller in monoecious than dioecious populations, because of constraints imposed on clone size by costs associated with geitonogamy; (ii) in dioecious populations, male clones are larger and flower more often than female clones because of sex‐differential reproductive costs. Differences in clone size and flowering could result in discordance between ramet‐ and genet‐based sex ratios. We used spatially explicit sampling to address these hypotheses in 10 monoecious and 11 dioecious populations of S. latifolia at the northern range limit in Eastern North America. In contrast to our predictions, monoecious clones were significantly larger than dioecious clones, probably due to their higher rates of vegetative growth and corm production, and in dioecious populations, there was no difference in clone size between females and males; ramet‐ and genet‐based sex ratios were therefore highly correlated. Genotypic diversity declined with latitude for both sexual systems, but monoecious populations exhibited lower genotypic richness. Differences in life history between the sexual systems of S. latifolia appear to be the most important determinants of clonal structure and diversity.     

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。     

Reproductive effort and costs of reproduction do not explain female-biased sex ratios in the moss Pseudocalliergon trifarium (Amblystegiaceae)

A fundamental assumption in life-history theory is that reproduction is costly. Higher reproductive investment for fruits than for flowers may result in larger costs of reproduction in females than in males, which is often used to explain male-skewed sex ratios in unisexual seed plants. In contrast, bryophytes have predominantly female-biased sex ratios, suggested to be a product of a higher average cost of sexual reproduction in males. Empirical evidence to support this notion is largely lacking. We investigated sex-specific reproductive effort and costs in the unisexual moss Pseudocalliergon trifarium that has a female-dominated expressed sex ratio and rarely produces sporophytes. Annual vegetative segment mass did not differ among male, female, and non-expressing individuals, indicating that there was no threshold-size for sex expression. Mean and annual mass of sexual branches were higher in females than in males, but branch number per segment did not differ between sexes. Prefertilization reproductive effort for females was significantly greater (11.2%) than for males (8.6%). No cost for sexual branch production in terms of reduced relative vegetative growth or decreased investment in reproductive structures in consecutive years was detected. A higher realized reproductive cost in males cannot explain the unbalanced sex ratio in the study species.     

Size-dependent resource allocation among vegetative propagules and male and female functions in the forest herb Laportea bulbifera

Reproductive resource investment among vegetative propagules and male and female sexual function and their size-dependence were investigated in a perennial forest herb, Laportea bulbifera . A theoretical model based on fitness gain curves predicts that optimal investments in three reproductive modes will increase with plant size if fitness returns in all three modes increase but become saturated with investment. In a field population, large plants of L. bulbifera produced both male and female inflorescences with propagules, while small plants produced only vegetative propagules. Biomass of propagules, male inflorescences, and infructescences with achenes were all positively correlated with plant size. The increase in investment with plant size was larger for propagule production than for sexual reproduction. The relationship between propagule biomass and plant size was constant irrespective of year, while the relationship between the biomass of sexual reproductive organs and plant size differed between two successive years. Annual change of individual sex expression was investigated for 25 transplanted plants. Although each plant changed its sex expression variously among male, female and bisexual from year to year, 23 out of 25 plants produced both male and female inflorescences in at least one year. The number of viable (germinated and survived) offspring from seeds was not significantly different from the number from propagules. The production cost of a propagule was higher than that of a seed. Resource allocation theory does not seem to be applicable to size-dependent resource allocation, especially the allocation between seeds and propagules in this species.     

Do sexual dimorphisms in reproductive allocation and new shoot biomass increase with an increase of altitude? A case of the shrub willow Salix reinii (Salicaceae)

Based on the general tendency for females of dioecious plants to pay higher reproductive cost than males, it has been predicted that females should have much more reduced reproductive outputs and diminished vegetative production than males in energy-limited habitats. Nevertheless, this prediction has rarely been directly investigated. We investigated altitudinal changes in reproductive biomass and shoot production, normalized by plant size, for females and males of a shrub willow, Salix reinii, on Mt. Hakkoda, northeast Japan. Females maintained higher reproductive biomass than males at all altitudes; however, reproductive allocation for both sexes tended to decrease at a similar rate with an increase in altitude. Moreover, females vegetatively produced at the same rate as males at all altitudes. These findings suggest that females have a mechanism to compensate for the extra investment in reproduction irrespective of a changing environment. Shoot production did not change with altitude, suggesting that S. reinii gave priority to vegetative investment at the cost of reproductive output at higher altitudes. Inconsistent with general predictions, females did not respond more sensitively than males to severe environmental conditions in either reproductive allocation or shoot production, despite much higher resource investment in reproduction.     

PATTERNS OF RESOURCE ALLOCATION IN A DIOECIOUS CAREX (CYPERACEAE)

Allocation to vegetative growth and sexual reproduction was investigated throughout the growing season in the dioecious sedge, Carex picta, under natural conditions and following experimental manipulations. Measurements taken on unmanipulated plants showed that the sexes did not differ in the total amount of biomass they allocated to either growth or reproduction. The relatively equal investment in reproduction by the two sexes is contrary to other studies, the majority of which show greater investment in reproduction by females. Two features of the reproductive biology of C. picta may account for the equal investment: the fruit are relatively inexpensive because they are uniovulate and nonfleshy, and the stamens are relatively expensive because C. picta is wind pollinated. In contrast to the lack of differences in the amount of allocation, there were differences between the sexes in the timing of allocation to growth and reproduction: males allocated more to reproduction and less to growth up to the time of flowering, whereas females showed this pattern during the time of fruit maturation. Defoliation and inflorescence removal experiments showed that a trade-off within plants between growth and reproduction does exist. In addition, the defoliation experiment revealed a difference in the response of the two sexes: defoliated tillers on males showed a reduction in growth, whereas defoliated tillers on females did not. Overall, the data support the idea that differences in the timing of reproductive expenditure are as important as the amount of expenditure in determining many aspects of the life history strategies of the two sexes.     

Sex Ratios and Resource Allocation among Sexually Reproducing Plants of Rubus chamaemorus

Sex ratios and patterns of size variation and resource allocationwere investigated in the dioecious species Rubus chamaemorus.Sex ratios among flowering ramets varied from 6% to 40% of females.Female ramets were slightly, although not significantly, tallerthan males. It appeared that population effects (including bothgenetic population and environmental site effects) on plantsize and allocation patterns at flowering are considerably greaterthan sex effects. If both flowering and fruit production areconsidered, then female allocation to reproduction clearly exceedsmale allocation. In females, no significant relationship wasdetected between the mass of reproductive and vegetative tissues,while males did exhibit such a relationship. Reproductive effortwas less for tall males than for small males. Despite the occurrence of sexual reproduction, the main modeof reproduction in R. chamaemorus is vegetative propagation,which is the best strategy for reproduction in the unpredictableclimate of high latitudes but which leads to skewed sex ratios.As a consequence of vigorous vegetative reproduction, individualclones can grow to be large. The results of electrophoreticstudies show that the numbers of clones per population are low.Copyright1994, 1999 Academic Press Rubus chamaemorus, cloudberry, sex ratios, resource allocation, clonal structure, electrophoresis     

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.     

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.