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1.
In terrestrial plants the segregation of male and female reproductions on different individuals results in the seed-shadow handicap: males do not disperse any seed so that the number of local patches reached by seeds is potentially reduced in dioecious populations in comparison to hermaphrodite populations. An analytical model, incorporating a lottery-based recruitment and dispersal stochasticity, was built. The spatially mediated cost of the seed-shadow handicap has been assessed considering the criterions for the invasion of a resident hermaphrodite species by a dioecious species and the reverse invasion, both species having the same demographic parameters but assuming a likely higher fecundity for dioecious females. The reciprocal invasion of a dioecious and hermaphrodite species differing only by their fecundity is never possible. The seed-shadow handicap disappears when the dispersal or survival rate is high enough. This latter point is due to dispersal stochasticity, which allows for the existence of empty patches. A low fecundity and an aggregated seed distribution increase dispersal stochasticity and increase the positive impact of a low mortality rate on the relative competitivity of dioecy and hermaphroditism. Adding a dispersal cost has a comparable effect but also requires higher dispersal rates for the dioecious invasion.  相似文献   

2.
Abstract.— Recent evidence has suggested that clades of dioecious angiosperms have fewer extant species on average than those of cosexual (hermaphroditic and monoecious) relatives. Reasons for the decrease in speciation rates and/or increase in extinction rates are only beginning to be investigated. One possibility is that dioecious species suffer a competitive disadvantage with cosexuals because only half of the individuals in a dioecious population are seed bearing. When only females produce seed, offspring will be more spatially clumped and will experience more local resource competition than when every individual produces seed. We examine two spatially explicit models to determine the effect of a reduction in seed dispersers on the invasibility and persistence of dioecious populations. Even though dioecious females were allowed to produce twice as many seeds as cosexuals, our results show that a reduction in the number of seed dispersers causes a decrease in the ability of dioecious progeny to find uninhabited sites, thus reducing persistence times. These results suggest that the maintenance of dioecy in the presence of hermaphroditic competitors requires a substantial increase in relative fitness and/or a large dispersal advantage of dioecious seeds.  相似文献   

3.

Background

The ‘gynodioecy–dioecy pathway’ is considered to be one of the most important evolutionary routes from hermaphroditism to separate sexes (dioecy). Despite a large accumulation of evidence for female seed fertility advantages in gynodioecious species (females and hermaphrodites coexist) in support of the first step in the gynodioecy–dioecy pathway, we still have very little evidence for the second step, i.e. the transition from gynodioecy to dioecy.

Scope

We review the literature to evaluate whether basic predictions by theory are supported. To establish whether females'' seed fertility advantage and frequencies are sufficient to favour the invasion of males, we review these for species along the gynodioecy–dioecy pathway published in the last 5 years. We then review the empirical evidence for predictions deriving from the second step, i.e. hermaphrodites'' male fertility increases with female frequency, selection favours greater male fertility in hermaphrodites in gynodioecious species, and, where males and hermaphrodites coexist with females (subdioecy), males have greater male fertility than hermaphrodites. We review how genetic control and certain ecological features (pollen limitation, selfing, plasticity in sex expression and antagonists) influence the trajectory of a population along the gynodioecy–dioecy pathway.

Conclusions

Females tend to have greater seed fertility advantages over hermaphrodites where the two coexist, and this advantage is positively correlated with female frequency across species, as predicted by theory. A limited number of studies in subdioecious species have demonstrated that males have an advantage over hermaphrodites, as also predicted by theory. However, less evidence exists for phenotypic selection to increase male traits of hermaphrodites or for increasing male function of hermaphrodites in populations with high female frequency. A few key case studies underline the importance of examining multiple components of male fertility and the roles of pollen limitation, selfing and plasticity, when evaluating advantages. We conclude that we do not yet have a full understanding of the transition from gynodioecy to dioecy.  相似文献   

4.
Aim The factors affecting the distribution of dioecious species have received surprisingly little attention and, as a consequence, are poorly understood. For example, there is a well‐documented negative association between dioecy and latitude, for which we have no candidate mechanisms. Conversely, it has been suggested that the relative proportion of dioecious species should be positively correlated with changes in elevation. Location Costa Rica, Central America. Methods We made use of data on the distribution of 175 seed plant species from a series of plots along a transect in Costa Rica that ranged from 30 to 2600 m a.s.l. to test the prediction that dioecy is correlated with elevation. Specifically, we examined relationships between the proportion of dioecy, at the species and individual levels, and the elevation, species richness, number of individuals, and phylogenetic diversity (PD) of plots. For comparison, we repeated all analyses with monoecious species, which also have unisexual flowers but do not suffer from reduced mate assurance and the seed shadow effect that may be the outcomes of having spatially separated sexes. Results The relative proportions of dioecious species and individuals displayed a unimodal relationship with elevation, both peaking at 750 m a.s.l. In contrast, the relative proportions of monoecious species and individuals displayed negative associations with elevation. In addition, the proportion of dioecious species was significantly positively associated with species richness and with the PD of plots. The proportion of monoecious species was not associated with species richness and was weakly positively associated with the PD of plots. Main conclusions Our results suggest that the selection pressure of elevation on the pollinators and life‐history strategy of dioecious species is much less than expected, and is overshadowed by the as‐yet unexplained correlation of dioecy with species richness. Additional studies of the ecology of cosexual and unisexual (i.e. dioecious and monoecious) species along large environmental gradients are needed.  相似文献   

5.
Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.  相似文献   

6.
Sex‐specific investment in pathogen resistance and immunity has been widely reported in animals and to a much lesser degree in plants. Here, we investigated the incidence of fungal pathogens in dioecious versus hermaphroditic plant species. We found that direct studies on differences between males and females in disease resistance or pathogen incidence were rare or non‐existent in plants, but if we made the prediction that if such differences exist (e.g. if males are less resistant than females), dioecious species should have a higher variation in pathogen diversity than hermaphrodites. Comparative studies on paired dioecious and hermaphrodite species from multiple plant families showed that hermaphrodites had a higher average pathogen load than dioecious species, consistent with the idea that higher outcrossing is beneficial to resistance to a greater diversity of pathogens. There was however no support for dioecious species also having a greater variance in pathogen diversity. Our results are consistent with dioecy providing a benefit in terms of pathogen resistance, but the data were insufficient to resolve if the male and female plants showed sex‐specific investment in resistance.  相似文献   

7.
The flowers and inflorescences of animal-pollinated dioecious plants are generally small and inconspicuous in comparison with outcrossing cosexual species. The net benefits of an attractive floral display may be different for dioecious compared to cosexual populations because dioecious species experience a more severe reduction in pollen delivery when pollinators forage longer on fewer individuals. Here, we develop a model that predicts the decrease in pollen delivery in dioecious relative to cosexual populations from female-female, female-male and male-male visit sequences as the number of individuals visited varies. To evaluate the predictions of our model we conducted a common garden experiment with dioecious and monoecious (cosexual) arrays of the insect-pollinated herb Sagittaria latifolia. We find that, although increasing the advertisements of floral rewards (i.e. increasing floral display) attracts more pollinators to individuals, the probability that these pollinators subsequently deliver pollen to neighbouring plants depends on sexual system. Because the number of individual plants visited per foraging trip did not increase significantly with floral display, the relative pollination success of dioecious versus monoecious populations decreases with increased floral display. We propose that this could explain why dioecy is strongly correlated with reduced floral display among angiosperm species.  相似文献   

8.
Interactions among multiple species form complex networks of interdependences and are considered primary factors in the generation and maintenance of biodiversity. Pteropodid bats are keystone species that provide important ecosystem services of pollination and seed dispersal in the tropics and subtropics. In this study, we investigated the utilization and preference of food resources by the insular frugivorous flying fox Pteropus dasymallus. We found that fig species constituted the major portion of the diet of the flying fox (94.6%). When foraging, the flying fox preferred seed figs from female trees over gall figs from male trees in functionally dioecious fig species. Germination experiments showed a significantly higher percentage of germination for fig seeds in feces than those from pellets and ripe figs (feces: 80.2%, pellets: 23.4%, ripe figs: 32.9%). Considering the active selection of seed figs and avoidance of gall figs by foraging flying foxes, we suggest that the abundance of seed figs accurately represents food availability for dioecy. This preference for seed figs or viable seeds can effectively promote the survival of pollinating wasps and might reinforce the evolution of dioecism in figs. In addition, the effects of gut passage on seed germination, in combination with the capacity of flying foxes to travel long distances, may substantially contribute to the efficiency of flying foxes as seed dispersers.  相似文献   

9.
The life history of figs (Ficus, Moraceae) involves pollination by specialized insects and seed dispersal by vertebrate frugivores. This three-way interaction raises the possibility of conflict between pollinators and seed dispersers over fig resources. The conflict might be mediated in dioecious figs by the segregation of inflorescences with specialized male and female sexual functions, termed gall figs and seed figs, on separate trees. In dioecious figs, pollinators are intimately associated with gall figs, whereas vertebrate frugivores prefer seed figs and disperse the seeds they contain. Optimal foraging theory predicts that frugivore preference for ripe seed figs is associated with superior nutritional quality when compared to gall figs. We tested this prediction comparing nutrient and mineral properties of ripe figs in 12 functionally dioecious and two monoecious species from New Guinea. Analyses of variance indicated that gall figs contain more fiber and minerals, whereas seed figs contain significantly more carbohydrates and fat. Fruit bats, the primary dispersers of dioecious figs in New Guinea, prefer carbohydrate-rich diets, and from this perspective, seed figs offer a greater nutritional reward than gall figs. More nondigestible fiber in gall figs than seed figs would appear to discourage frugivory. Parallel differences between ripe gall figs and seed figs occur in each independent dioecious lineage whereas nutritional content in monoecious figs is more similar to seed figs. This suggests that sexual dimorphism in nutritional quality might be adaptive and associated with the maintenance of functional dioecy in figs.  相似文献   

10.
  • Revealing the environmental pressures determining the frequency of females amongst populations of sexually dimorphic plants is a key research question. Analyses of sex ratio variation have been mainly done in dioecious plants, which misses key plant sexual systems that might represent intermediate stages in the evolution of dioecy from hermaphroditism.
  • We investigated female frequency across populations of sexually dimorphic plant species in relation to environmental stressors (temperature, precipitation), totaling 342 species, 2011 populations, representing 40 orders and three different sexual systems (dioecy, gynodioecy and subdioecy). We also included the biome where the population was located to test how female frequency may vary more broadly with climate conditions.
  • After correcting for phylogeny, our results for gynodioecious systems showed a positive relationship between female frequency and increased environmental stress, with the main effects being temperature‐related. Subdioecious systems also showed strong positive relationships with temperature, and positive and negative relationships related to precipitation, while no significant effects on sex ratio in dioecious plants were detected.
  • Combined, we show that female frequencies in an intermediate sexual system on the pathway from hermaphroditism to dioecy respond strongly to environmental stressors and have different selective agents driving female frequency.
  相似文献   

11.
Documenting the floral biology and breeding system of species throughout the Rubiaceae family provides data on the number of times heterostyly and dioecy may have evolved in this large family. The objectives of this paper are to quantify (a) whether Chassalia corallioides , a small tree endemic to La Reunion Island in the Indian Ocean, is another example of the evolution of dioecy from distyly and (b) whether reproductive traits linked to male and female function vary over the ecological distribution of this species. Quantification of pollen production and fruit set following controlled and natural pollinations demonstrate that this species is dioecious. Male flowers have longer corolla tubes than female flowers. Female flowers have long styles with stigmas placed above the anthers whereas males have short styles with stigmas placed below the anthers. Stigmas and anthers are reciprocally placed in each morph, illustrating that the species is morphologically heterostylous. Both fecundity and flower size are negatively correlated with altitude. In male plants, corollas are shorter and wider and anthers are placed closer to the mouth of the corolla tube with increasing altitude. Male plants flowered more often than female plants, the likely cause of the male biased sex ratio in each of the two years studied. The evolution of dioecy in relation to the island biogeography of the region and the diversification of the genus Chassalia is discussed.  相似文献   

12.
Androdioecy is an unusual breeding system in which populations consist of separate male and hermaphrodite individuals. The evolution of androdioecy is still poorly understood; however, there is evidence from several androdioecious species that the breeding system may have evolved from dioecy (males and females). This article presents a simple deterministic model showing that androdioecy can evolve from dioecy under a broad range of realistic conditions. For the evolution of androdioecy from dioecy, hermaphrodites must be able to invade the dioecious population. Then, males must be maintained, while females are eliminated. Hermaphrodite invasion is favored when females are pollen limited and hermaphrodites have high overall fertility and are self-fertile. Male maintenance is favored when hermaphrodites resemble females, having high seed production and low pollen fitness, and when the selfing rate is not too high. These conditions were satisfied over a broad and realistic range of parameter values, suggesting that the evolution of androdioecy from dioecy is highly plausible.  相似文献   

13.
The role of mutations of small versus large effect in adaptive evolution is of considerable interest to evolutionary biologists. The major evolutionary pathways for the origin of dioecy in plants (the gynodioecy and monoecy-paradioecy pathways) are often distinguished by the number of mutations involved and the magnitude of their effects. Here, we investigate the genetic and environmental determinants of sex in Sagittaria latifolia, a species with both monoecious and dioecious populations, and evaluate evidence for the evolution of dioecy via gynodioecy or monoecy-paradioecy. We crossed plants of the two sexual systems to generate F1, F2 and backcross progeny, and grew clones from dioecious populations in low-and high-fertilizer conditions to examine sex inconstancy in females and males. Several lines of evidence implicate two-locus control of the sex phenotypes. In dioecious populations sex is determined by Mendelian segregation of alleles, with males heterozygous at both the male- and female-sterility loci. In monoecious populations, plants are homozygous for alleles dominant to male sterility in females and recessive to female sterility in males. Experimental manipulation of resources revealed sex inconstancy in males but not females. These results are consistent with predictions for the evolution of dioecy via gynodioecy, rather than the expected monoecy-paradioecy pathway, given the ancestral monoecious condition.  相似文献   

14.
Dioecy has evolved independently, many times, among unrelated taxa. It also appears to have evolved along two contrasting pathways: (1) from hermaphroditism via monoecy to dioecy and (2) from hermaphroditism via gynodioecy to dioecy. Most dioecious plants have close cosexual relatives with some means of promoting outcrossing (e.g., herkogamy, dichogamy, self-incompatibility, or monoecy). To the extent that these devices prevent inbreeding, the evolution of dioecy in these species cannot logically be attributed to selection for outcrossing. In these cases, the evolution of dioecy is, we believe, due to selection for sexual specialization. However, in other species, that lack outbreeding close relatives, dioecy may have evolved from gynodioecy (males and hermaphrodites) as an outbreeding device. Subsequent disruptive selection and selection for sexual specialization may have also shaped the evolution of dioecy from gynodioecy in these species, resulting in two genetically determined, constant sex morphs. Both pathways for the evolution of dioecy require the operation of disruptive selection, though the gynodioecy route involves more restrictive disruptive selection and a genetic designation of gender. In contrast, the monoecy route is not dependent on the genetic designation of two sex morphs, but, rather, allows the possibility of sexual intermediates and sexual lability. Both pathways produce one morph in which maleness is suppressed and another in which the female function is negligible or nonexistent—the reproductive mode recognized as dioecy. Evidence is presented here to support the thesis that instances of sexual lability, the presence of an array of sexual intermediates, sex-switching, and sexual niche segregation can be explained in terms of the pathway that was taken in the evolution of a particular dioecious species. In addition, the degree of sexual dimorphism seen in dioecious species is correlated with mode of pollination (insector wind-pollinated) and other ecological factors.  相似文献   

15.
The size advantage hypothesis (SAH) predicts that the rate of increase in male and female fitness with size (the size advantage) drives the evolution of sequential hermaphroditism or sex change. Despite qualitative agreement between empirical patterns and SAH, only one comparative study tested SAH quantitatively. Here, we perform the first comparative analysis of sex change in Labridae, a group of hermaphroditic and dioecious (non–sex changer) fish with several model sex‐changing species. We also estimate, for the first time, rates of evolutionary transitions between sex change and dioecy. Our analyses support SAH and indicate that the evolution of hermaphroditism is correlated to the size advantage. Furthermore, we find that transitions from sex change to dioecy are less likely under stronger size advantage. We cannot determine, however, how the size advantage affects transitions from dioecy to sex change. Finally, contrary to what is generally expected, we find that transitions from dioecy to sex change are more likely than transitions from sex change to dioecy. The similarity of sexual differentiation in hermaphroditic and dioecious labrids might underlie this pattern. We suggest that elucidating the developmental basis of sex change is critical to predict and explain patterns of the evolutionary history of sequential hermaphroditism.  相似文献   

16.
We have reanalyzed models of the breakdown of dioecy involving modified males to investigate female frequencies in the resulting gynodioecious populations. We extend and simplify previous treatments to deal with biologically relevant factors including pollen limitation, partial selfing of modified males, and inbreeding depression, to highlight the different empirically detectable advantages that may be gained by modified males that can reproduce as cosexes (i.e., can produce some seeds); these include “inconstant males,” which can sometimes display some female function. Males reproducing wholly or occasionally as cosexual phenotypes can gain the transmission advantage of selfing, if partial self‐fertilization is possible, and from reproductive assurance when pollen is limiting. If, because of resource limitation, such cosexual phenotypes produce fewer ovules than females, their nonselfed ovules will require a lower pollen pool size for full seed‐set, compared with females. We investigate the conditions for these benefits to allow modified males to invade dioecious populations. Sometimes, such invasion leads to replacement of dioecy by the cosexual type, but sometimes the breakdown populations remain sexually polymorphic. When competition occurs between genotypes in the pollen load on a flower, high female frequencies can arise when Y chromosome‐bearing pollen competes poorly with X pollen.  相似文献   

17.
Abstract The evolution of dioecy was studied in Schiedea (Caryophyllaceae), a genus endemic to the Hawaiian Islands. Eight of the 22 species are diclinous, possessing gynodioecious, subdioecious, or dioecious breeding systems. A biogeographic analysis of the genus indicates that the ancestor of Schiedea colonized early in the history of the Hawaiian Islands. Subsequently, hermaphroditic species appear to have engaged in inter-island colonization more frequently than diclinous species. For this reason, single-island endemism and dicliny are more common on the older Hawaiian Islands. Strong inbreeding depression was detected in three species of Schiedea , indicating that genetic factors have played a role in the evolution of dicliny. Depending on the level of natural selfing, the expression of inbreeding depressioin may have favored the outcrossed progeny of rare females in populations, and eventually the evolution of dioecy. In contrast to evidence for inbreeding depression, there was very little evidence that resource allocation, sex lability, or habitat partitioning have played an important role in the evolution of dioecy. In subdioecious S. globosa hermaphrodites were largely male in function, and in gynodioecious S. salicaria females and hermaphrodites were equivalent in nearly all aspects of female function that could be measured. Variation in breeding systems in Schiedea and the closely related Alsinidendron may result from the past history of population bottlenecks that have resulted in varying levels of inbreeding depression.  相似文献   

18.
About 15,000 angiosperm species (∼6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy.  相似文献   

19.
Examinations of breeding system transitions have primarily concentrated on the transition from hermaphroditism to dioecy, likely because of the preponderance of this transition within flowering plants. Fewer studies have considered the reverse transition: dioecy to hermaphroditism. A fruitful approach to studying this latter transition can be sought by studying clades in which transitions between dioecy and hermaphroditism have occurred multiple times. Freshwater crustaceans in the family Limnadiidae comprise dioecious, hermaphroditic and androdioecious (males + hermaphrodites) species, and thus this family represents an excellent model system for the assessment of the evolutionary transitions between these related breeding systems. Herein we report a phylogenetic assessment of breeding system transitions within the family using a total evidence comparative approach. We find that dioecy is the ancestral breeding system for the Limnadiidae and that a minimum of two independent transitions from dioecy to hermaphroditism occurred within this family, leading to (1) a Holarctic, all‐hermaphrodite species, Limnadia lenticularis and (2) mixtures of hermaphrodites and males in the genus Eulimnadia. Both hermaphroditic derivatives are essentially females with only a small amount of energy allocated to male function. Within Eulimnadia, we find several all‐hermaphrodite populations/species that have been independently derived at least twice from androdioecious progenitors within this genus. We discuss two adaptive (based on the notion of ‘reproductive assurance’) and one nonadaptive explanations for the derivation of all‐hermaphroditism from androdioecy. We propose that L. lenticularis likely represents an all‐hermaphrodite species that was derived from an androdioecious ancestor, much like the all‐hermaphrodite populations derived from androdioecy currently observed within the Eulimnadia. Finally, we note that the proposed hypotheses for the dioecy to hermaphroditism transition are unable to explain the derivation of a fully functional, outcrossing hermaphroditic species from a dioecious progenitor.  相似文献   

20.
The evolution of dioecy, heterodichogamy, and labile sex expression in Acer   总被引:1,自引:0,他引:1  
The northern hemisphere tree genus Acer comprises 124 species, most of them monoecious, but 13 dioecious. The monoecious species flower dichogamously, duodichogamously (male, female, male), or in some species heterodichogamously (two morphs that each produce male and female flowers but at reciprocal times). Dioecious species cannot engage in these temporal strategies. Using a phylogeny for 66 species and subspecies obtained from 6600 nucleotides of chloroplast introns, spacers, and a protein-coding gene, we address the hypothesis (Pannell and Verdú, Evolution 60: 660-673. 2006) that dioecy evolved from heterodichogamy. This hypothesis was based on phylogenetic analyses (Gleiser and Verdú, New Phytol. 165: 633-640. 2005) that included 29-39 species of Acer coded for five sexual strategies (duodichogamous monoecy, heterodichogamous androdioecy, heterodichogamous trioecy, dichogamous subdioecy, and dioecy) treated as ordered states or as a single continuous variable. When reviewing the basis for these scorings, we found errors that together with the small taxon sample, cast doubt on the earlier inferences. Based on published studies, we coded 56 species of Acer for four sexual strategies, dioecy, monoecy with dichogamous or duodichogamous flowering, monoecy with heterodichogamous flowering, or labile sex expression, in which individuals reverse their sex allocation depending on environment-phenotype interactions. Using Bayesian character mapping, we infer an average of 15 transformations, a third of them involving changes from monoecy-cum-duodichogamy to dioecy; less frequent were changes from this strategy to heterodichogamy; dioecy rarely reverts to other sexual systems. Contra the earlier inferences, we found no switches between heterodichogamy and dioecy. Unexpectedly, most of the species with labile sex expression are grouped together, suggesting that phenotypic plasticity in Acer may be a heritable sexual strategy. Because of the complex flowering phenologies, however, a concern remains that monoecy in Acer might not always be distinguishable from labile sex expression, which needs to be addressed by long-term monitoring of monoecious trees. The 13 dioecious species occur in phylogenetically disparate clades that date back to the Late Eocene and Oligocene, judging from a fossil-calibrated relaxed molecular clock.  相似文献   

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