Phylogenetic insights into the correlates of dioecy in meadow-rues (Thalictrum, Ranunculaceae)

Numerous studies have examined the evolution of sexual systems in angiosperms, but few explore the interaction between these and the evolution of pollination mode. Wind pollination is often associated with unisexual flowers, but which evolved first and played a causative role in the evolution of the other is unclear. Thalictrum, meadow-rues (Ranunculaceae), provides a unique opportunity to study the evolution of these traits because it contains insect and wind pollination and four sexual systems. We used a phylogenetic approach to reconstruct ancestral states for sexual system, pollination mode, and geographic distribution in Thalictrum, and tested for correlations to uncover the factors involved in the evolution of unisexuality and wind pollination. Our results show that dioecy, andro- and gynomonoecy evolved at least twice from hermaphroditism. Wind pollination, unisexual flowers, and New World distribution were all significantly correlated. Wind pollination may have evolved early in the genus, followed by multiple losses and gains, and likely preceded the origin of unisexual flowers in several cases; we found no evidence for unisexual flowers evolving prior to wind pollination. Given a broad scale study showing the evolution of dioecy before wind pollination, our results from a finer scale analysis highlight that different evolutionary pathways are likely to occur throughout angiosperms.     

Phylogenetic analysis of the ecological correlates of dioecy in angiosperms

We report on a phylogenetic analysis of correlations between the occurrence of dioecy and several ecological and life-history attributes: tropical distribution, woody growth form, abiotic pollination, small inconspicuous flowers and inflorescences, many-flowered inflorescences and fleshy fruits. Various hypotheses have been proposed to explain why associations occur between dioecy and several of these attributes, yet most assume that dioecy originates more often in clades with these traits than in clades with alternative character states. To investigate correlations between dioecy and these attributes, and to provide insights into the potential evolutionary pathways that have led to these associations, we assigned states of these traits to genera on a large-scale molecular phylogeny of the angiosperms; we then used maximum-likelihood analysis to analyse the presence of correlations and the sequence of acquisition of traits. Phylogenetic analysis revealed correlations between dioecy and six of the seven attributes; only many-flowered inflorescences exhibiting no association with the dioecious condition. The particular correlations that were revealed and the strength of the association differed among the three main monophyletic groups of angiosperms (Rosids, Asterids, and Eumagnoliids). Our analysis provided no general support for the hypothesis that dioecy is more likely to evolve in lineages already possessing the seven attributes we considered. Further analysis of the intercorrelations of the seven attributes provided evidence for non-independence between some of the traits, implying that functional associations among these traits have influenced the ecology and evolution of dioecious species.     

Incidence of dioecy in relation to growth form,pollination and dispersal

Summary Recent theories predict the evolution of dioecy among higher plants, in association with certain pollination and fruit dispersal traits. However, reported associations of dioecy with pollination, dispersal and growth form traits have not distinguished the effects of each trait separately, controlling for the others. Because these traits are associated among themselves, existing analyses may involve spurious or indirect correlations. This paper reports the incidence of dioecy in a subarctic and an arctic flora, and analyzes the occurrence of dioecy among vascular plants classified jointly by growth form, floral (pollination) syndrome, and fruit (dispersal) syndrome. Dioecism is no more frequent in the arctic flora as a whole, but its incidence increases northward among woody plants. This increase is associated with an increase in the proportion of woody species having small, inconspicuous flowers, and not with the syndrome of fleshy or animal dispersed fruits. Within the floras of Alaska, California, and the Northeastern US, dioecy is markedly more frequent among woody plants and among plants having small, inconspicuous flowers, and that is the only strong statistical association of dioecy for the species of these floras. When genera and families are analyzed similarly, dioecy is also associated significantly with dispersal syndrome. Thus, among angiosperms, evidence currently does not support either an uniquely strong or exclusive association of dioecy with dispersal traits, as it does for gymnosperms (Givnish 1980). It is extremely desirable to analyze the occurrence of dioecy among taxa classified jointly by all relevant ecological traits, rather than analyzing marginal distributions.     

Explaining the distribution of breeding and dispersal syndromes in conifers

The evolution of plants exhibiting different sexes, or dioecy, is correlated with a number of ecological and life-history traits such as woody growth form and animal-dispersed seeds, but the underlying causes of these associations are unclear. Previous work in seed plants has suggested that the evolution of fleshy cones or seeds may favour dioecy. In this study, we use a well-sampled molecular phylogeny of conifers to show that although dioecy and fleshiness strongly co-occur at the species level, this relationship has not resulted from numerous separate origins of this trait combination or from differential rates of diversification. Instead, we suggest that two character combinations—the ancestral dry-monoecious condition and the derived fleshy-dioecious condition—have persisted in conifers longer than other combinations over evolutionary time. The persistence of these trait combinations appears to reflect differences in the rate of successful transition into and out of these character states over time, as well as the geographical restriction of species with rare combinations and their consequent vulnerability to extinction. In general, we argue that such persistence explanations should be considered alongside ‘key innovation’ hypotheses in explaining the phylogenetic distribution of traits.     

Sexual specialization and inbreeding avoidance in the evolution of dioecy

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.     

Sexual dimorphism and the genetic potential for evolution of sex allocation in the gynodioecious plant, Schiedea salicaria

Sex allocation theory addresses how separate sexes can evolve from hermaphroditism but little is known about the genetic potential for shifts in sex allocation in flowering plants. We tested assumptions of this theory using the common currency of biomass and measurements of narrow-sense heritabilities and genetic correlations in Schiedea salicaria, a gynodioecious species under selection for greater differentiation of the sexes. Female (carpel) biomass showed heritable variation in both sexes. Male (stamen) biomass in hermaphrodites also had significant heritability, suggesting the potential for further evolution of dioecy. Significant positive genetic correlations between females and hermaphrodites in carpel mass may slow differentiation between the sexes. Within hermaphrodites, there were no negative genetic correlations between male and female biomass as assumed by models for the evolution of dioecy, suggesting that S. salicaria is capable of further changes in biomass allocation to male and female functions and evolution toward dioecy.     

The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy

Abstract.— Seed dormancy plays an important role in germination ecology and seed plant evolution. Morphological seed dormancy is caused by an underdeveloped embryo that must mature prior to germination. It has been suggested that the presence of an underdeveloped embryo is plesiomorphic among seed plants and that parallel directional change in embryo morphology has occurred separately in gymnosperms and in angiosperms. We test these hypotheses using original data on embryo morphology of key basal taxa, a published dataset, and the generalized least squares (GLS) method of ancestral character state reconstruction. Reconstructions for embryo to seed ratio (E:S) using family means for 179 families showed that E:S has increased between the ancestral angiosperm and almost all extant angiosperm taxa. Species in the rosid clade have particularly large embryos relative to the angiosperm ancestor. Results for the gymnosperms show a similar but smaller increase. There were no statistically significant differences in E:S between basal taxa and any derived group due to extremely large standard errors produced by GLS models. However, differences between reconstructed values for the angiosperm ancestor and more highly nested nodes are large and these results are robust to topological and branch-length manipulations. Our analysis supports the idea that the underdeveloped embryo is primitive among seed plants and that there has been a directional change in E:S within both angiosperms and gymnosperms. Our analysis suggests that dormancy enforced by an underdeveloped embryo is plesiomorphic among angiosperms and that nondormancy and other dormancy types probably evolved within the angiosperms. The shift in E:S was likely a heterochronic change, and has important implications for the life history of seed plants.     

被子植物性系统的多样性、生态功能及分布规律

性系统是被子植物繁育系统的核心, 决定着植物种群的遗传特征、进化方向与速度, 在种群动态、群落结构及生态系统的构建与维持中具有重要意义。本文回顾了被子植物性系统的发展历程及研究方向, 总结了近30年基于性系统研究的前沿科学问题, 包括性系统的多样性和进化、与其他功能性状的生态关联、沿环境梯度的分布格局及变化规律、与群落物种共存机制和群落动态的关系及其对干扰的响应。尽管有关植物性系统的研究已经延伸到生态学领域的诸多方面, 有力地推动了各方面的发展, 但仍有很多值得关注和需要着重研究的方向和问题。本文对未来基于植物性系统的研究方向等提出了展望, 并指出, 在当前全球气候变化背景下, 性系统可作为重要的功能性状应用于指导生物多样性保护和生态系统管理政策的制定。     

Dioecy,Monoecy, and Their Ecological Correlates in the Littoral Forest of Madagascar

Dioecy is a rare breeding system in flowering plants, but one that has evolved multiple times in different plant lineages. Dioecious species are commonly associated with several ecological traits, including woody habit, fleshy fruit, and small, inconspicuous flowers, although the significance of these correlations has been debated extensively. Monoecy is a breeding system that may lead to the evolution of dioecy, but ecological correlates of monoecious species have rarely been analyzed. We determined the diversity of breeding systems in the littoral forests of Madagascar and used multivariate methods to estimate which ecological traits have the strongest association with dioecy and are the best predictors of breeding systems. The Malagasy littoral forest flora is a well‐documented subset of the Malagasy flora, with 13 percent of total species diversity in an area <1 percent of the island's total. We found high levels of dioecy (18.4%) and monoecy (9.2%), similar to incidences in other tropical floras. Using multinomial logistic regression, dioecy has the strongest association with woody habit and fleshy fruit. Monoecious species have a strong association with small flowers, although this association does not hold at higher taxonomic levels. Using classification and regression tree (CART) methods, the best predictors of dioecy are woody habit and fleshy fruit; monoecy is equally predicted by fleshy and dry fruit. For the Malagasy littoral forest, both methods provide further support for the importance of woody habit and fleshy fruit in the evolution of dioecy.     

Present day risk of extinction may exacerbate the lower species richness of dioecious clades

Dioecious clades have been observed to have lower species richness than their non‐dioecious sister groups indicating that dioecious species experience higher extinction rates and (or) lower speciation rates. To determine whether current threats to biodiversity may exacerbate this pattern, we examined the threat to exclusively dioecious families of angiosperms among the 13,013 species of threatened plants included in the IUCN Red List of Threatened Species. When examined phylogenetically, dioecious families had proportionally more species listed than their sister groups. We then examined whether ecological traits correlated with dioecy, namely tropical distribution, woody growth form, and fleshy fruits, are associated with having higher proportions of threatened species. Ignoring breeding system, woody growth form was the only trait that was associated with a greater than expected proportion of threatened species per family. Red‐Listed dioecious families were more likely to have a woody growth form than non‐dioecious families. Woody growth habit is likely contributing to the higher incidence of dioecious species being at risk of extinction but is not solely responsible for the pattern because higher risk within dioecious groups was also apparent in a comparison of exclusively woody sister‐group pairs. Our results indicate that dioecious plants may warrant special attention in conservation practices.     

Multiple nuclear gene phylogenetic analysis of the evolution of dioecy and sex chromosomes in the genus Silene

In the plant genus Silene, separate sexes and sex chromosomes are believed to have evolved twice. Silene species that are wholly or largely hermaphroditic are assumed to represent the ancestral state from which dioecy evolved. This assumption is important for choice of outgroup species for inferring the genetic and chromosomal changes involved in the evolution of dioecy, but is mainly based on data from a single locus (ITS). To establish the order of events more clearly, and inform outgroup choice, we therefore carried out (i) multi-nuclear-gene phylogenetic analyses of 14 Silene species (including 7 hermaphrodite or gynodioecious species), representing species from both Silene clades with dioecious members, plus a more distantly related outgroup, and (ii) a BayesTraits character analysis of the evolution of dioecy. We confirm two origins of dioecy within this genus in agreement with recent work on comparing sex chromosomes from both clades with dioecious species. We conclude that sex chromosomes evolved after the origin of Silene and within a clade that includes only S. latifolia and its closest relatives. We estimate that sex chromosomes emerged soon after the split with the ancestor of S. viscosa, the probable closest non-dioecious S. latifolia relative among the species included in our study.     

Repeated evolution of dioecy from androdioecy in Acer

The evolution of breeding systems was studied in the genus Acer, with special attention to the origin of androdioecy and dioecy, using a phylogenetic approach. Parsimony and maximum-likelihood techniques were used to infer the ancestral character state and trends in the evolution of breeding systems. Information on breeding systems was obtained from the literature, and phylogenetic relationships were taken from three published phylogenies. Although a general trend from duodichogamy to dioecy through heterodichogamy has been proposed for the genus Acer, our results show that a general trend is not detected when phylogenetic relationships are taken into account. Dioecy appeared as a derived state that evolved at least three times and never reversed towards other states. Three different paths to dioecy have been followed in the genus Acer: from heterodichogamous androdioecy; from heterodichogamous trioecy; and from dichogamous subdioecy. Therefore, although the best documented cases of evolution of androdioecy indicate that this breeding system evolves from dioecy, in the genus Acer the opposite situation occurs (androdioecy leading to dioecy). Here we discuss the role of inbreeding avoidance and sexual specialization as selective forces driving the evolution of dioecy in the genus Acer.     

On the rarity of dioecy in flowering plants

Dioecy, the coexistence of separate male and female individuals in a population, is a rare but phylogenetically widespread sexual system in flowering plants. While research has concentrated on why and how dioecy evolves from hermaphroditism, the question of why dioecy is rare, despite repeated transitions to it, has received much less attention. Previous phylogenetic and theoretical studies have suggested that dioecy might be an evolutionary dead end. However, recent research indicates that the phylogenetic support for this hypothesis is attributable to a methodological bias and that there is no evidence for reduced diversification in dioecious angiosperms. The relative rarity of dioecy thus remains a puzzle. Here, we review evidence for the hypothesis that dioecy might be rare not because it is an evolutionary dead end, but rather because it easily reverts to hermaphroditism. We review what is known about transitions between hermaphroditism and dioecy, and conclude that there is an important need to consider more widely the possibility of transitions away from dioecy, both from an empirical and a theoretical point of view, and by combining tools from molecular evolution and insights from ecology.     

Reproductive trait variation in the functionally dioecious and morphologically heterostylous island endemic Chassalia corallioides (Rubiaceae)

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.     

An angiosperm-wide analysis of the gynodioecy–dioecy pathway

Background and Aims

About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precursors of this sexual system are thought to be monoecy and gynodioecy. A previous angiosperm-wide study revealed that many dioecious species have evolved through the monoecy pathway; some case studies and a large body of theoretical research also provide evidence in support of the gynodioecy pathway. If plants have evolved through the gynodioecy pathway, gynodioecious and dioecious species should co-occur in the same genera. However, to date, no large-scale analysis has been conducted to determine the prevalence of the gynodioecy pathway in angiosperms. In this study, this gap in knowledge was addressed by performing an angiosperm-wide survey in order to test for co-occurrence as evidence of the gynodioecy pathway.

Methods

Data from different sources were compiled to obtain (to our knowledge) the largest dataset on gynodioecy available, with 275 genera that include at least one gynodioecious species. This dataset was combined with a dioecy dataset from the literature, and a study was made of how often dioecious and gynodioecious species could be found in the same genera using a contingency table framework.

Key Results

It was found that, overall, angiosperm genera with both gynodioecious and dioecious species occur more frequently than expected, in agreement with the gynodioecy pathway. Importantly, this trend holds when studying different classes separately (or sub-classes, orders and families), suggesting that the gynodioecy pathway is not restricted to a few taxa but may instead be widespread in angiosperms.

Conclusions

This work complements that previously carried out on the monoecy pathway and suggests that gynodioecy is also a common pathway in angiosperms. The results also identify angiosperm families where some (or all) dioecious species may have evolved from gynodioecious precursors. These families could be the targets of future small-scale studies on transitions to dioecy taking phylogeny explicitly into account.     

植物雌雄异株性别决定研究进展

植物中雌雄性别分化是一种进化的性状。雌雄异株在多个开花植物谱系中独立演化, 但各个支系的性染色体状态、性别决定区域与性别决定基因不尽相同。多样的植物性染色体和性别决定系统为研究植物性别相关基因的形成机制、性别决定区域和性染色体进化提供了极好的机会。随着测序技术的进步和分析方法的提高, 近年来越来越多物种性别决定的相关分子机制得到解析, 并将理论成果应用于提升经济效益与城市环境等实际问题中。本文将从目前的研究现状和方法, 性别决定单、双基因模型的建立, 植物性染色体进化过程等方面进行总结, 对未来植物性别决定的研究提出四点建议: (1)研究方向逐步从基因研究扩展到调控途径研究; (2)从单一物种转向相关科属比较研究; (3)改进现有性别决定基因模型或探索新模型和性别模式物种; (4)加强性别鉴定技术在实际生产中的研发工作。同时探讨性别决定理论研究未来在农业生产、园艺绿化种植中幼苗性别鉴别筛选等方面的应用前景。     

Origins of flower morphology

Flowers evolved in many steps, probably starting long before flowering plants (angiophytes) originated. Certain parts of flowers are conservative and have not changed much during evolution; others are evolutionarily highly plastic. Here conservative features are discussed and an attempt is made to trace them back through their evolutionary history. Microsporangia and ovules (which develop into seeds) are preangiophyte floral elements. Angiospermy, combined with postgenital fusion, was the most prominent key innovation in angiophytes. Angiospermy and thecal organization of stamens originated earlier than all clades of extant angiosperms (the crown group of angiophytes). Differentiation of a perianth into calyx and corolla and syncarpy appeared after the first branching of the basalmost clades of extant angiosperms. Sympetaly and floral tubes as well as tenuinucellar, unitegmic ovules originated as major innovations in the clade that led to asterids. An obvious trend in flower evolution is increased synorganisation of parts, which led to new structures. Fixation of floral organ number and position was a precondition for synorganization. Concomitantly, plasticity changed from number and position of organs to shape of the new structures. Character distribution mapped onto cladograms indicates that key innovations do not appear suddenly, but start with trials and only later become deeply rooted genetically in the organization. This is implied from the common occurrence of reversals in the early history of an innovation. J. Exp. Zool. (Mol. Dev. Evol.) 291:105-115, 2001.     

Sex determination through X–Y heterogamety in Salix nigra

The development of non-recombining sex chromosomes has radical effects on the evolution of discrete sexes and sexual dimorphism. Although dioecy is rare in plants, sex chromosomes have evolved repeatedly throughout the diversification of angiosperms, and many of these sex chromosomes are relatively young compared to those found in vertebrates. In this study, we designed and used a sequence capture array to identify a novel sex-linked region (SLR) in Salix nigra, a basal species in the willow clade, and demonstrated that this species has XY heterogamety. We did not detect any genetic overlap with the previously characterized ZW SLRs in willows, which map to a different chromosome. The S. nigra SLR is characterized by strong recombination suppression across a 2 MB region and an excess of low-frequency alleles, resulting in a low Tajima’s D compared to the remainder of the genome. We speculate that either a recent bottleneck in population size or factors related to positive or background selection generated this differential pattern of Tajima’s D on the X and autosomes. This discovery provides insights into factors that may influence the evolution of sex chromosomes in plants and contributes to a large number of recent observations that underscore their dynamic nature.Subject terms: Plant evolution, Quantitative trait     

A COMPARATIVE ANALYSIS OF SEX CHANGE IN LABRIDAE SUPPORTS THE SIZE ADVANTAGE HYPOTHESIS

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.