Development and Evolution of Unisexual Flowers: A Review

The development of unisexual flowers has been described in a large number of taxa, sampling the diversity of floral phenotypes and sexual systems observed in extant angiosperms, in studies focusing on floral ontogeny, on the evo-devo of unisexuality, or on the genetic and chromosomal bases of unisexuality. We review here such developmental studies, aiming at characterizing the diversity of ontogenic pathways leading to functionally unisexual flowers. In addition, we present for the first time and in a two-dimensional morphospace a quantitative description of the developmental rate of the sexual organs in functionally unisexual flowers, in a non-exhaustive sampling of angiosperms with contrasted floral morphologies. Eventually, recommendations are provided to help plant evo-devo researchers and botanists addressing macroevolutionary and ecological issues to more precisely select the taxa, the biological material, or the developmental stages to be investigated.

Disentangling the effects of jasmonate and tissue loss on the sex allocation of an annual plant

Selection through pollinators plays a major role in the evolution of reproductive traits. However, herbivory can also induce changes in plant sexual expression and sexual systems, potentially influencing conditions governing transitions between sexual systems. Previous work has shown that herbivory has a strong effect on sex allocation in the wind-pollinated annual plant Mercurialis annua, likely mediated by resource loss. It is also known that many plants respond to herbivory by inducing signalling, and endogenous responses to it, via the plant hormone jasmonate. Here, we attempt to uncouple the effects of herbivory on sex allocation in M. annua through resource limitation (tissue loss) versus plant responses to jasmonate hormone signalling. We used a two-factorial experiment with four treatment combinations: control, herbivory (25% chronic tissue loss), jasmonate, and combined herbivory and jasmonate. We estimated the effects of tissue loss and defence-inducing hormones on reproductive allocation, male reproductive effort, and sex allocation. Tissue loss caused plants to reduce their male reproductive effort, resulting in changes in combined sex allocation. However, application of jasmonate after herbivory reversed its effect on male investment. Our results show that herbivory has consequences on plant sex expression and sex allocation, and that defence-related hormones such as jasmonate can buffer the impacts. We discuss the physiological mechanisms that might underpin the effects of herbivory on sex allocation, and their potential implications for the evolution of plant sexual systems.

Taxonomy and Relationships Within Polemonium foliosissimum (Polemoniaceae): Untangling a Clade of Colorful and Gynodioecious Herbs

Abstract— New molecular and ecological data have necessitated taxonomic revisions of several species complexes within Polemonium (Polemoniaceae), including P. foliosissimum, an herbaceous perennial widespread in the Intermountain West of the United States. As currently circumscribed, P. foliosissimum is a highly polymorphic species of four taxonomic varieties. One of the most striking morphological traits of the species is its diversity in flower color, which is unusual for the genus. Several species have been proposed based on this variation in flower color. However, these names have been treated as infraspecific taxa because previous authors have concluded that the presence of micropollen grains throughout the geographic range of the species complex indicated partial hybrid sterility and therefore incomplete barriers to gene flow. However, recent evidence suggests that micropollen is instead due to a gynodioecious breeding system. Using 128 nuclear loci and eight quantitative morphological traits, I clarify relationships and taxonomy within the species complex. I show that what is currently circumscribed as four varieties of P. foliosissimum represent five species that, in addition to differing in corolla color, differ in leaflet number, corolla size, and vegetative and floral pubescence. I propose a new species endemic to the White Mountains of southeastern Arizona, Polemonium apachianum. This study provides a new phylogenetic context and taxonomic circumscription to serve as a framework for future research on the evolution of floral color and sexual systems in a previously misunderstood but evolutionarily exciting system.

Hermaphroditism in fish: incidence, distribution and associations with abiotic environmental factors

The distribution of hermaphroditism in fishes has traditionally been mainly explained by its dependence on biotic factors. However, correlates with major abiotic factors have not been investigated on a quantitative basis and at a global scale. Here, we determined the incidence of hermaphroditism in fish at the family and species level, tested the hypothesis that evolutionary relationships account for the poor presence of hermaphroditism in freshwater species, and tested the association of sexual systems with latitude, habitat type and depth. Functional hermaphroditism is reported in 8 orders, 34 families and 370 species of fishes, all teleosts. Sequential hermaphroditism predominates over simultaneous hermaphroditism at a ratio ~ 5:1 and protogyny (female-to-male sex change) predominates ~ 6:1 over protandry (male-to-female). We found 12 hermaphroditic species that can live in freshwater. However, seven of these species are from four primarily marine families while there are only five species from two mostly freshwater families. Protogynous and bi-directional sex changers have a tighter association with reef-associated tropical and subtropical habitats when compared to protandrous species, which tend to be more plastic in terms of distribution requirements. Finally, simultaneous hermaphrodite species live both in the deep sea and shallow waters in similar proportions. This study can be the basis for further research in specific groups for different purposes, including ecological and evolutionary issues as well as conservation and management of exploited species. Understanding the environmental correlates can help to forecast changes in the distribution or phenology of hermaphrodites in a global change scenario.

Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems

The hypothesis that epigenetic mechanisms of gene expression regulation have two main roles in vertebrate sex is presented. First, and within a given generation, by contributing to the acquisition and maintenance of (i) the male or female function once during the lifetime in individuals of gonochoristic species; and (ii) the male and female function in the same individual, either at the same time in simultaneous hermaphrodites, or first as one sex and then as the other in sequential hermaphrodites. Second, if environmental conditions change, epigenetic mechanisms may have also a role across generations, by providing the necessary phenotypic plasticity to facilitate the transition: (i) from one sexual system to another, or (ii) from one sex-determining mechanism to another. Furthermore, if the environmental change lasts enough time, epimutations could facilitate assimilation into genetic changes that stabilize the new sexual system or sex-determining mechanism. Examples supporting these assertions are presented, caveats or difficulties and knowledge gaps identified, and possible ways to test this hypothesis suggested. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

SELECTION DRIVES THE EVOLUTION OF CONVERGENT GENE EXPRESSION CHANGES DURING TRANSITIONS TO CO-SEXUALITY IN HAPLOID SEXUAL SYSTEMS

Co-sexuality has evolved repeatedly from ancestors with separate sexes across a wide range of taxa. The switch to co-sexuality is expected to involve major molecular readjustments at the level of gene expression patterns, as modified males or females will express the opposite sexual function for which their phenotypes have been optimized. However, the molecular changes underpinning this important transition remain unknown, particularly in organisms with haploid sexual systems such as bryophytes, red and brown algae. Here, we explore four independent events of emergence of co-sexuality from uni-sexual (dioicous) ancestors in brown algal clades in order to examine the nature, evolution and degree of convergence of gene expression changes that accompany the breakdown of dioicy. The amount of male versus female phenotypic differences in dioicous species were not correlated with the extent of sex-biased gene expression, in strike contrast to what is observed in animals. Although sex-biased genes exhibited a high turnover rate during brown alga diversification, their predicted functions were remarkably conserved. Transition to co-sexuality consistently involved adaptive gene expression shifts and rapid sequence evolution, particularly of male-biased genes. The gene expression profiles of co-sexual species were more similar to those of females than to males of related dioicous species, suggesting that the former may have arisen from ancestral females. Finally, we identified extensive convergent gene expression changes associated with the transition to co-sexuality, and these changes appear to be driven by selection. Together, our observations provide novel insights on how co-sexual systems arise from ancestral, haploid UV sexual systems.

Switching it up: algal insights into sexual transitions

While the process of meiosis is highly conserved across eukaryotes, the sexual systems that govern life cycle phase transitions are surprisingly labile. Switches between sexual systems have profound evolutionary and ecological consequences, in particular for plants, but our understanding of the fundamental mechanisms and ultimate causes underlying these transitions is still surprisingly incomplete. We explore here the idea that brown and green algae may be interesting comparative models that can increase our understanding of relevant processes in plant reproductive biology, from evolution of gamete dimorphism, gametogenesis, sex determination and transitions in sex-determining systems.

Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia

The diversity of mating and sexual systems in Angiosperms is spectacular, but the factors driving their evolution remain poorly understood. In plants of the Oleaceae family, an unusual self-incompatibility (SI) system has been discovered recently, whereby only two distinct homomorphic SI specificities segregate stably. To understand the role of this peculiar SI system in preventing or promoting the diversity of sexual phenotypes observed across the family, an essential first step is to characterize the genetic architecture of these two traits. Here, we developed a high-density genetic map of the androdioecious shrub P. angustifolia based on a F1 cross between a hermaphrodite and a male parent with distinct SI genotypes. Using a double restriction-site associated digestion (ddRAD) sequencing approach, we obtained reliable genotypes for 196 offspring and their two parents at 10,388 markers. The resulting map comprises 23 linkage groups totaling 1,855.13 cM on the sex-averaged map. We found strong signals of association for the sex and SI phenotypes, that were each associated with a unique set of markers on linkage group 12 and 18 respectively, demonstrating inheritance of these traits as single, independent, mendelian factors. The P. angustifolia linkage map shows robust synteny to the olive tree genome overall. Two of the six markers strictly associated with SI in P. angustifolia have strong similarity with a recently identified 741kb chromosomal region fully linked to the SI phenotype on chromosome 18 of the olive tree genome, providing strong cross-validation support. The SI locus stands out as being markedly more rearranged, while the sex locus has remained relatively more collinear. This P. angustifolia linkage map will be a useful resource to investigate the various ways by which the sex and SI determination systems have co-evolved in the broader phylogenetic context of the Oleaceae family.

Living apart if you can – how genetically and developmentally controlled sex has shaped the evolution of liverworts

Sexual differentiation in bryophytes occurs in the dominant gametophytic generation. Over half of bryophytes are dioicous, and this pattern in liverworts is even more profound as over 70% of species are dioicous. However, the evolutionary mechanisms leading to the prevalence of dioicy and the shifts of sexual systems between dioicy and monoicy have remained poorly known. These essential factors in reproductive biology are explored here in light of phylogenetics combined with evidence of genomic characterization of sex chromosomes and sex-determination, as well as cytology. Our analyses and discussions on liverworts are focused on: (1) ancestry and shifts in sexuality, (2) evolution of sex chromosomes and maintenance of haploid dioicy, and (3) environmental impact on the evolution of monoicism. We show that the dioicous condition is ancestral in liverworts, and the evolution of sexual systems is both conserved and stable with an ancient origin, but also highly dynamic in certain more recently diverged lineages. We assume that the haploid dioicy maintained in the course of evolution must be linked to the genetically controlled sex-determination, and transition from genetically to developmentally controlled sex determination, the evolution of monoicism, is driven by ephemeral and unstable environments. Monoicy is less stable in the long-term than dioicy, and thus, ultimately, dioicy is selected in liverworts. It is concluded that sexual dimorphism is maintained through a highly dynamic evolutionary process, sex chromosomes bearing distinct set of evolutionary forces that can have large impacts on genome evolution and may also promote speciation.