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.     

Selfish male‐determining element favors the transition from hermaphroditism to androdioecy

According to the current, widely accepted paradigm, the evolutionary transition from hermaphroditism toward separate sexes occurs in two successive steps: an initial, intermediate step in which unisexual individuals, male or female, sterility mutants coexist with hermaphrodites and a final step that definitively establishes dioecy. Two nonexclusive processes can drive this transition: inbreeding avoidance and reallocation of resources from one sexual function to the other. Here, we report results of controlled crosses between males and hermaphrodites in Phillyrea angustifolia, an androdioecious species with two mutually intercompatible, but intraincompatible groups of hermaphrodites. We observed different segregation patterns that can be explained by: (1) epistatic interactions between two unlinked diallelic loci, determining sex and mating compatibility, and (2) a mutation with pleiotropic effects: female sterility, full compatibility of males with both hermaphrodite incompatibility groups, and complete male‐biased sex‐ratio distortion in one of the two groups. Modeling shows that these mechanisms can explain the high frequency of males in populations of P. angustifolia and can promote the maintenance of androdioecy without requiring inbreeding depression or resource reallocation. We thus argue that segregation distortion establishes the right conditions for the evolution of cryptic dioecy and potentially initiates the evolution toward separate sexes.     

Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism

One evolutionary pathway from plants with combined male and female functions (hermaphroditism) to those with separate sexes (dioecy) involves females coexisting with hermaphrodites (gynodioecy). The research presented here explores sex allocation in Fragaria virginiana (a gynodioecious wild strawberry), within the context of theory on the gynodioecy–dioecy transition. By growing clonally replicated plants in the greenhouse and surveying six populations in situ, I evaluated the effects of plant size, genotype, sexual identity, population of origin and female frequency on sex allocation. I found significant positive effects of plant size on most sex allocation traits studied. In addition to strong sex-specific allocation patterns, I found significant broad-sense heritabilities for all traits, suggesting that plants could respond to selection. Moreover, there was a negative genetic correlation between pollen production and fruit set per flower within hermaphrodites, lending support to a basic assumption of sex allocation theory. On the other hand, several sex allocation traits, namely pollen and ovules per flower in hermaphrodites, were positively genetically correlated, suggesting that they may act to constrain the evolution of sexual dimorphism. Populations differed in the frequency of females, and females were more prevalent on sites with lower soil moisture and where hermaphrodites were least likely to produce fruit, suggesting that females’ seed fitness relative to that of hermaphrodites may be strongly environment-dependent in this species.     

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.     

Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.     

Consequences of inbreeding depression due to sex-linked loci for the maintenance of males and outcrossing in branchiopod crustaceans.

Androdioecy, where males co-occur with hermaphrodites, is a rare sexual system in plants and animals. It has a scattered phylogenetic distribution, but it is common and has persisted for long periods of evolutionary time in branchiopod crustaceans. An earlier model of the maintenance of males with hermaphrodites in this group, by Otto et al. (1993), considered the importance of male-hermaphrodite encounter rates, sperm limitation, male versus hermaphrodite viability and inbreeding depression suffered by selfed progeny. Here I advance this model in two ways: (1) by exploring the conditions that would allow the invasion of hermaphrodites into a dioecious population and that of females into an androdioecious population; and (2) by incorporating a term that accounts for the potential effects of genetic load linked to a dominant hermaphrodite-determining allele in androdioecious populations. The new model makes plausible sense of observations made in populations of the species Eulimnadia texana, one of a number of related species whose common ancestor evolved hermaphroditism (and androdioecy) from dioecy. In particular, it offers an explanation for the long evolutionary persistence of androdioecy in branchiopods and suggests reasons for why dioecy has not re-evolved in the clade. Finally, it provides a rather unusual illustration of the implications of the degeneration of loci linked to a sex-determining locus.     

Low potential for sexual selection in simultaneously hermaphroditic animals

Hermaphroditic animals are poorly represented in the sexual selection literature. This deficiency may reflect our inability to come to grips with hermaphroditism or, alternatively, it could be due to an inherent difference between hermaphrodites and gonochorists. Here we provide a number of reasons why sexual selection on traits related to mate acquisition can be expected to be intrinsically weaker in hermaphrodites. We show that the ''male'' fitness component, which can be increased by sexual selection in hermaphrodites, is only half that of pure males in a gonochorist population. This component can be reduced even further when hermaphrodites self-fertilize. As a result, the potential for sexual selection (ψ) on male characters in hermaphrodites is at most half that of gonochorists. Given a specific mate handling cost, sperm production cost and rate of encountering receptive mates, we calculate the optimal allocation to mate acquisition and sperm. Since both partners of a hermaphroditic pair invest in mate acquisition, hermaphrodites should optimally invest less in mate acquisition. This can further reduce ψ by up to one-half. A higher readiness to mate and high investment in sperm can lead to a further systematic reduction in P_s in hermaphrodites.     

Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene

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.     

The role of hybridization in the evolution of sexual system diversity in a clonal,aquatic plant

The stable coexistence within populations of females, males, and hermaphrodites (subdioecy) is enigmatic because theoretical models indicate that maintenance of this sexual system involves highly restricted conditions. Subdioecy is more commonly interpreted as a transitory stage along the gynodioecious pathway from hermaphroditism to dioecy. The widespread, North American, aquatic plant Sagittaria latifolia is largely composed of monoecious or dioecious populations; however, subdioecious populations with high frequencies of hermaphrodites (mean frequency = 0.50) characterize the northern range boundary of dioecy in eastern North America. We investigated two hypotheses for the origin of subdioecy in this region. Using polymorphic microsatellite loci, we evaluated whether subdioecy arises through selection on standing genetic variation for male sex inconstancy in dioecious populations, or results from hybridization between monoecious and dioecious populations. We found evidence for both pathways to subdioecy, although hybridization was the more common mechanism, with genetic evidence of admixture in nine of 14 subdioecious populations examined. Hybridization has also played a role in the origin of androdioecious populations in S. latifolia, a mechanism not often considered in the evolution of this rare sexual system. Our study demonstrates how hybridization has the potential to play a role in the diversification of plant sexual systems.     

A comparative study of sperm morphology, cytology and activation in Caenorhabditis elegans, Caenorhabditis remanei and Caenorhabditis briggsae

Studies of sterile mutants in Caenorhabditis elegans have uncovered new insights into fundamental aspects of gamete cell biology, development, and function at fertilization. The genome sequences of C. elegans, Caenorhabditis briggsae and Caenorhabditis remanei allow for informative comparative studies among these three species. Towards that end, we have examined wild-type sperm morphology and activation (spermiogenesis) in each. Light and electron microscopy studies reveal that general sperm morphology, organization, and ultrastructure are similar in all three species, and activation techniques developed for C. elegans were found to work well in both C. briggsae and C. remanei. Despite important differences in the reproductive mode between C. remanei and the other two species, most genes required for spermiogenesis are conserved in all three. Finally, we have also examined the subcellular distribution of sperm epitopes in C. briggsae and C. remanei that cross-react with anti-sera directed against C. elegans sperm proteins. The baseline data in this study will prove useful for the future analysis and interpretation of sperm gene function across nematode species.     

Gynodioecy to dioecy: are we there yet?

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.     

Differences in female reproductive success between female and hermaphrodite individuals in the subdioecious shrub Eurya japonica (Theaceae)

Subdioecy is thought to occupy a transitional position in the gynodioecy–dioecy pathway, explaining one of the evolutionary routes from hermaphroditism to dioecy. Quantifying any female reproductive advantage of females versus hermaphrodites is fundamental to examining the spectrum between subdioecy and dioecy; however, this is challenging, as multiple interacting factors, such as pollen limitation and resource availability, affect plant reproduction. We compared the female reproductive success of females and hermaphrodites via a field experiment in which we hand‐pollinated individuals of the subdioecious shrub Eurya japonica of similar size growing under similar light conditions. Effects of pollen limitation and seed quality were also evaluated through comparing the results of hand‐ and natural‐pollination treatments and performing additional laboratory and greenhouse experiments. Overall, females had higher fruit set and produced heavier fruit and more seeds than hermaphrodites, and these results were more pronounced for hand‐pollinated than for natural‐pollinated plants of both sexes. We also found that seeds naturally produced by females had a higher mean germination rate. These results indicate that females had a pronounced advantage in female reproductive success under conditions of no pollen limitation. The sexual difference in the degree of pollen limitation suggests a pollinator‐mediated interaction, whereas the higher female reproductive success of females even under natural conditions implies that E. japonica is a good model species for elucidating the later stages of the gynodioecy–dioecy pathway.     

Pollen limitation and the evolution of androdioecy from dioecy

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.     

RECURRENT EVOLUTION OF DIOECY IN BRYOPHYTES

The origin and maintenance of separate sexes (dioecy) is an enduring evolutionary puzzle. Although both hermaphroditism and dioecy occur in many diverse clades, we know little about the long‐term evolutionary consequences of changing sexual system. Here we find evidence for at least 133 transitions between sexual systems in mosses, representing an almost unparalleled lability in the evolution of their sexual systems. Furthermore, in contrast to predictions, the transition rate from hermaphroditism to dioecy was approximately twice as high as the reverse transition. Our results also suggest that hermaphrodites may have higher rates of diversification than dioecious mosses. These results illustrate the utility of mosses for understanding the genomic and macroevolutionary consequences of hermaphroditism and dioecy.     

Do tiny males grow up? Sperm competition and optimal resource allocation schedule of dwarf males of barnacles

Barnacles, marine crustaceans, have three sexual patterns: simultaneous hermaphroditism, dioecy and androdioecy. In dioecy and androdioecy, large individuals (females and hermaphrodites, respectively) are attached by dwarf males. Depending on species, some dwarf males grow up, others do not in their life time. To investigate which environmental conditions affect growth patterns of dwarf males of barnacles, we investigate the evolutionarily stable life history strategy of dwarf males using Pontryagin's maximum principle. Sperm competition among dwarf males and that among dwarf males and large hermaphrodites is taken into account. Dwarf males grow up in food-rich environments, while they do not grow at all in food-poor environments. ESS of the resource allocation schedule between reproduction and growth follows an "intermediate growth strategy" (simultaneous growth and reproduction) for dioecious species, in which sperm competition is not severe. On the other hand, it approaches "bang-bang control" (switching from allocating all resources toward growth then to reproduction), as sperm competition against surrounding large hermaphrodites becomes severe in androdioecious species.     

The Evolution of Hermaphroditism from Dioecy in Crustaceans: Selfing Hermaphroditism Described in a Fourth Spinicaudatan Genus

The evolution of reproductive systems has intrigued evolutionary biologists for well over a century. Recent empirical and theoretical work has elucidated the evolution of dioecy (separate males and females) from hermaphroditism in many plant species. The reverse transition, evolving hermaphroditism from dioecy, has occurred many times in animals, and yet is poorly studied relative to its reverse analog in plants. Crustaceans in the sub-order Spinicaudata have evolved hermaphroditism from dioecy three separate times, in some cases forming all-hermaphroditic species and in others forming androdioecious (males + hermaphrodites) species. Herein we report evidence of hermaphroditism in a fourth spinicaudatan genus: the newly described Calalimnadia. We present sex ratio and anatomical evidence that Calalimnadia mahei comprises selfing hermaphrodites, with no males being found in over 10,000 offspring reared. We combine these reproductive results with those of other Spinicaudata to estimate the evolution of hermaphroditism in this crustacean sub-order. We use these genetic data combined with anatomical evidence to suggest that C. mahei represents a fourth, independent derivation of hermaphroditism from dioecy in these reproductively labile crustaceans.     

Two sexes,one body: intra‐ and intersex covariation of gamete phenotypes in simultaneous hermaphrodites

By harboring male and female functions in the same genome and expressing them in every individual, simultaneous hermaphrodites may incur sexual conflict unless both sex functions can evolve phenotypic optima independently of each other. The first step toward understanding their capacity to do so lies in understanding whether sex functions are phenotypically correlated within individuals, but remarkably few data address this issue. We tested the potential for intra‐ and intersex covariation of gamete phenotypes to mediate sexual conflict in broadcast‐spawning hermaphrodites (the ascidians Ciona intestinalis and Pyura praeputialis), for which sex‐specific selection acts predominantly on sperm–egg interactions in the water column. In both species, gamete phenotypes covaried within and across sex functions, implying that selection may be unable to target them independently because its direct effects on male gametes translate into correlated effects on female gametes and vice versa. This alone does not preclude the evolution of a different phenotypic optimum for each sex function, but imposes the more restrictive requirement that selection – which ultimately sorts among whole individuals, not sex functions – aligns with the direction in which gamete phenotypes covary at this level.     

Tales of two snails: sexual selection and sexual conflict in Lymnaea stagnalis and Helix aspersa

Sexual selection and sexual conflict have been shown to playkey roles in the evolution of species with separate sexes. Experimentalevidence is accumulating that this is also true for simultaneoushermaphrodites. For example, many species of land snails forcefullystab their mating partners with love darts. In the brown gardensnail (Helix aspersa, now called Cantareus asperses), this dartincreases sperm storage and paternity, probably via the transferof an allohormone that inhibits sperm digestion. A recent interspeciescomparison of dart-possessing land snails revealed coevolutionbetween darts and spermatophore-receiving organs that is consistentwith counteradaptation against an allohormonal manipulation.The great pond snail (Lymnaea stagnalis) seems to use a seminalproduct to manipulate its partner and mates in the male rolewhen enough seminal fluid is available in the prostate gland.Receipt of semen not only initiates egg laying in virgin animals,but also feminizes the mating partner later in life. These increasesin the female function have been shown to go at the expenseof growth and seminal fluid production of the sperm recipient.Although in Helix, and probably also Lymnaea, the sperm donorbenefits from the induced changes through increased fertilizationsuccess, the sperm recipient may experience injury, imposedreallocation of resources, and altered sperm storage. Thesefindings support the existence of sexual conflict in simultaneouslyhermaphroditic snails, and its importance for the evolutionof mating behaviors and reproductive morphologies is discussed.     

Adaptive evolution of sperm bindin tracks egg incompatibility in neotropical sea urchins of the genus Echinometra

Bindin is a gamete recognition protein known to control species-specificsperm-egg adhesion and membrane fusion in sea urchins. Previousanalyses have shown that diversifying selection on bindin aminoacid sequence is found when gametically incompatible speciesare compared, but not when species are compatible. The presentstudy analyzes bindin polymorphism and divergence in the threeclosely related species of Echinometra in Central America: E.lucunter and E. viridis from the Caribbean, and E. vanbruntifrom the eastern Pacific. The eggs of E. lucunter have evolveda strong block to fertilization by sperm of its neotropicalcongeners, whereas those of the other two species have not.As in the Indo-West Pacific (IWP) Echinometra, the neotropicalspecies show high intraspecific bindin polymorphism in the samegene regions as in the IWP species. Maximum likelihood analysisshows that many of the polymorphic codon sites are under mildpositive selection. Of the fixed amino acid replacements, mosthave accumulated along the bindin lineage of E. lucunter. Weanalyzed the data with maximum likelihood models of variationin positive selection across lineages and codon sites, and withmodels that consider sites and lineages simultaneously. Ourresults show that positive selection is concentrated along theE. lucunter bindin lineage, and that codon sites with aminoacid replacements fixed in this species show by far the highestsignal of positive selection. Lineage-specific positive selectionparalleling egg incompatibility provides support that adaptiveevolution of sperm proteins acts to maintain recognition ofbindin by changing egg receptors. Because both egg incompatibilityand bindin divergence are greater between allopatric speciesthan between sympatric species, the hypothesis of selectionagainst hybridization (reinforcement) cannot explain why adaptiveevolution has been confined to a single lineage in the AmericanEchinometra. Instead, processes acting to varying degrees withinspecies (e.g., sperm competition, sexual selection, and sexualconflict) are more promising explanations for lineage-specificpositive selection on bindin.