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Transitions take on added significance when they are maintained through multiple speciation events and become characteristic features of lineages. Of particular interest are cases in which replicated character state transitions occur among unrelated lineages because this generally indicates similar selective mechanisms and functional convergence. Today, studies of reproductive transitions in flowering plants are the focus of considerable research in plant evolutionary biology reviewed in Barrett This interest arises because transitions affecting modes of reproduction have profound ecological and evolutionary consequences influencing genetic diversity within populations, phenotypic evolution and patterns of diversification.

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The three major evolutionary transitions in plant reproductive systems discussed in this article—the evolution of selfing from outcrossing, dioecy from hermaphroditism and wind pollination from animal pollination. SI refers to self-incompatibility. Note that in some transitions to selfing and dioecy the immediate ancestors may be wind pollinated.

The evolution of predominant self-fertilization autogamy from high levels of outcrossing is the most frequent reproductive transition in flowering plants Stebbins Autogamous species are well represented in many floras, especially those associated with Mediterranean climates, and among successful annual colonizers. There are no accurate estimates of the number of origins of selfing in angiosperms but it is probable that this transition has occurred many hundreds of times.

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Most transitions to autogamy are likely to go undetected because selfing lineages are often short-lived relative to those composed of outcrossing species. Not surprisingly, given the frequency of this transition and its genetic consequences, it has attracted more attention than any other shift in plant reproductive system reviewed in Uyenoyama et al. There are important biological reasons why the evolution of selfing from outcrossing is particularly intriguing to evolutionary biologists.

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Second, the shift to predominant selfing profoundly influences floral evolution, affecting the allocation of resources to floral display, pollen production and aspects of life history Charnov Third, selfing individuals can establish colonies at low density, or following long-distance dispersal, and therefore this ability has significant ecological, demographical and biogeographical implications Baker The two most general explanations for why selfing evolves are: i the advantage that selfing individuals have over outcrossers when pollinators or mates are scarce Darwin and ii the genetic transmission advantage through pollen that selfing variants experience because selfers are both the maternal and paternal parents of the seed they produce Fisher There is considerable biogeographical evidence indicating that selfing populations occupy range margins, ecologically marginal sites, or areas with reduced pollinator densities where outcrossers are absent, all circumstances predicted by the reproductive assurance hypothesis.

However, surprisingly few field studies have provided experimental evidence in support of the reproductive assurance hypothesis reviewed in Eckert et al. Moreover, even less work has been conducted on the automatic selection hypothesis. Future investigations are needed to determine the relative importance of these two hypotheses in explaining the evolution of selfing in plants. Heterostylous species provide valuable model systems for investigating the transition from outcrossing to selfing.

Heterostyly is a floral polymorphism in which populations are composed of two distyly or three tristyly mating morphs distinguished by the reciprocal arrangements of their sexual organs. This polymorphism promotes pollinator-mediated disassortative between morph mating and is maintained in populations by negative frequency-dependent selection.

In many heterostylous groups, obligate outcrossing, enforced by heteromorphic self-incompatibility, has been replaced by predominant selfing as a result of the origin of self-compatible homostyles with anthers and stigmas in close contact. The transition from outcrossing to selfing has been detected at the intraspecific level through studies of geographical variation see below , and by phylogenetic analysis and character mapping in groups with variable mating systems e.

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Schoen et al. The genetic mechanisms and evolutionary pathways responsible for the origin of selfing differ between these two genera.

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  • In contrast, in Eichhornia homostylous selfing forms arise initially through major gene changes to stamen position with subsequent polygenic modifiers reducing flower size Barrett et al. Hence, in heterostylous species, there is evidence for different genetic and developmental pathways for obtaining the same functional phenotype—plants with the capacity for autonomous self-pollination. Study systems discussed in the text that have been used for research on plant reproductive diversity. Plants with this morphology exhibit mixed mating. Note the conspicuous flower size dimorphism, a common feature of dioecious species.

    Ontario, Canada. The hermaphroditic inflorescence is from a monoecious population and has male flowers at the top of the inflorescence and female flowers at the bottom. The female and male inflorescences are from a dioecious population. This genus contains both animal- and wind-pollinated species. Inflorescences are protogynous with male flowers at the top and female flowers below. All photographs taken by the author. In both Turnera and Eichhornia , selfing homostyles tend to occupy geographical range margins, a pattern consistent with reproductive assurance. Homostyles in both groups have colonized Caribbean islands, undoubtedly because of the capacity of single individuals to found colonies.

    There is some evidence in Turnera that on large ecologically heterogeneous islands e.

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    A key issue in determining whether selfing is an evolutionary dead end concerns the degree of selfing considered. Highly selfing species e. On the other hand, in selfing species with moderate rates of outcrossing e. Determining if there is a threshold selfing rate beyond which the evolution of the selfing syndrome is inevitable would be valuable, and more generally work on the potential nonlinear relations between mating patterns, genetic diversity and selection response in plant populations is needed.

    Homostyles in Eichhornia , like Turnera , have arisen on multiple occasions and exhibit geographically marginal distributions. We have focused most of our attention on E. Populations in northeast Brazil are large flowered, primarily tristylous and outcrossing, whereas small-flowered autogamous populations occur on Jamaica, Cuba and in scattered localities in Nicaragua and Mexico; populations with mixed mating and intermediate flower sizes connect these extremes.

    Studies on the inheritance of mating-system modification, and comparisons of the genetic relationships of populations using nuclear DNA sequences, have provided evidence for multiple independent transitions to predominant selfing Barrett et al. Our work has shown that the joint action of stochastic forces and natural selection can destabilize tristyly causing the loss of morphs from populations and the subsequent spread of self-pollinating variants through automatic selection and reproductive assurance Barrett et al.

    The shift to selfing is an example of a transition in mating pattern triggered by genetic drift and fulfils some of the key conditions identified in Sewall Wright's shifting balance theory of evolutionary change Coyne et al. Our current work is examining the genomic consequences of replicated transitions from outcrossing to selfing in E. The evolution of populations with females and males dioecy from hermaphroditism has interested evolutionary biologists since Darwin struggled to understand the circumstances that might favour the unisexual condition in angiosperm species.

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    In immobile organisms, like plants, it is not immediately obvious why hermaphroditism should be abandoned in favour of unisexuality, because a reduction or loss of pollen vectors would severely compromise individual fitness. Another difficulty for the evolution of dioecy is that genetic transmission is halved for unisexuals in comparison with hermaphrodites, which can acquire fitness through either of two sexual avenues.

    Finally, for dioecy to evolve from hermaphroditism requires the spread of sterility mutations that under most circumstances would be deleterious to fitness. These hurdles present an intriguing puzzle for evolutionary biologists. Monoecy is the condition in which individual plants possess both female and male flowers. Disruptive selection on genetic variation in floral sex ratios could in principle result in female and male specialists. Dioecy is commonly associated with a suite of life history and reproductive traits.

    For example, unlike predominant selfing, dioecy occurs most commonly in long-lived species and is rare in annuals. Understanding the functional basis of these associations can provide useful clues about the ecological factors causing transitions to unisexuality. Using a molecular phylogeny of the angiosperms, and maximum likelihood approaches that take into account the phylogenetic non-independence of species, Vamosi et al. Why do these trait associations occur?

    Unfortunately, there are no clear answers to this question. This is because it has not been possible to determine with any confidence the order of acquisition of these traits in relation to the origins of dioecy. For example, is dioecy more likely to evolve in fleshy-fruited lineages, or does dioecy favour the evolution of fleshy fruits?

    These questions are difficult to answer because the presence of fleshy fruits is also correlated with woodiness, another correlate of dioecy. The intercorrelation of traits makes it tricky to tease apart the potential mechanisms involved in the evolution of dioecy. Future progress is more likely to come from analysing smaller-scale phylogenies of families or genera polymorphic for sexual systems and the traits of interest. However, finding groups that meet these criteria and have multiple independent transitions to dioecy will be challenging. In this study, the largest source of uncertainty was the interspersion of hermaphroditic and sexually dimorphic taxa across phylogenetic trees owing to the evolutionary lability of sexual systems in the genus.

    This diversity includes both the origin of dioecy and its reversion to hermaphroditism. Such variation complicates inferences on ancestral nodes and the determination of the statistical confidence of character state transitions. A particularly thorny issue came to light from sampling multiple populations of W.

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    The interest in these species arises because of their widespread distributions and the fact that they are both polymorphic for sexual-system variation with both hermaphroditic and gender dimorphic populations. Unexpectedly, and despite a recent taxonomic treatment of the group, both species were found to be non-monophyletic. Clearly, this situation makes the interpretation of character evolution uncertain. Investigators interested in character state transitions should sample widely to confirm species boundaries and the monophyly of species under investigation. Unfortunately, this is often not done in phylogenetic studies, especially in large groups where extensive taxon sampling is necessary.

    The most widely accepted hypothesis for the function of dioecy is that it is a mechanism of inbreeding avoidance preventing self-fertilization. Gender dimorphism commonly evolves from self-compatible rather than self-incompatible ancestors, a pattern consistent with the anti-selfing hypothesis.