BREAKDOWN OF DIOECY: MODELS WHERE MALES ACQUIRE COSEXUAL FUNCTIONS

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.     

Sexual systems and population genetic structure in an annual plant: testing the metapopulation model

The need for reproductive assurance during dispersal, along with the pressure of local mate competition, means that the importance of frequent or repeated colonization is implicit in the literature on sexual system evolution. However, there have been few empirical tests of the association between colonization history and sexual system in plants, and none within a single species. Here we use patterns of genetic diversity to provide such a test in the Mercurialis annua species complex, which spans the range of systems from self-compatible monoecy through androdioecy to dioecy. This variation has been hypothesized to result from differing patterns of metapopulation turnover and recolonization. Because monoecy should be favored during colonization, androdioecy and dioecy will be maintained only in regions with low rates of local extinction and recolonization, and these differences should also be reflected in patterns of neutral genetic diversity. We show that monoecious populations of M. annua display lower within-population genetic diversity than androdioecious populations and higher genetic differentiation than dioecious and androdioecious populations, as predicted by metapopulation models. In contrast, regional diversity in M. annua appears to be primarily a product of postglacial range expansion from two refugia in the eastern and western Mediterranean Basin.     

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.     

Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae)

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.     

Pollen Production in the Androdioecious Datisca glomerata (Datiscaceae): Implications for Breeding System Equilibrium

Abstract Androdioecy (the presence of males and hermaphrodites in a breeding population) is a rare reproductive system in plants, with Datisca glomerata (Datiscaceae) representing the only well-documented example. Recent reports of high outcrossing rates, inbreeding depression, and high male pollen production satisfy theoretical predictions for the continued maintenance of androdioecy in populations of this species. However, in prior studies pollen production was measured indirectly in terms of numbers of anthers per flower—based on the assumption that male and hermaphroditic plant have equal numbers of flowers and that anthers from the two sexual morphs produce equivalent amounts of pollen. Herein, we demonstrate that male and hermaphrodite plants do not differ significantly in terms of flower number, but that pollen production in anthers from hermaphroditic plants is 12.6% higher than in anthers from male plants, thus refining the estimate of relative pollen fecundity of male versus hermaphrodite plants. The differential lowers the frequency of males predicted by theory, but is still consistent with the maintenance of androdioecy in this species.     

Hybridization, polyploidy, and the evolution of sexual systems in Mercurialis (Euphorbiaceae)

Hybridization and polyploidy are widely believed to be important sources of evolutionary novelty in plant evolution. Both can lead to novel gene combinations and/or novel patterns of gene expression, which in turn provide the variation on which natural selection can act. Here, we use nuclear and plastid gene trees, in conjunction with morphological data and genome size measurements, to show that both processes have been important in shaping the evolution of the angiosperm genus Mercurialis, particularly a clade of annual lineages that shows exceptional variation in the sexual system. Our results indicate that hexaploid populations of M. annua, in which the rare sexual system androdioecy is common (the occurrence of males and hermaphrodites) is of allopolyploid origin involving hybridization between an autotetraploid lineage of M. annua and the related diploid species M. huetii. We discuss the possibility that androdioecy may have evolved as a result of hybridization between dioecious M. huetii and monoecious tetraploid M. annua, an event that brought together the genes for specialist males with those for hermaphrodites.     

Polyploidy and the sexual system: what can we learn from Mercurialis annua?

The evolutionary success of polyploidy most directly requires the ability of polyploid individuals to reproduce and transmit their genes to subsequent generations. As a result, the sexual system (i.e. the mating system and the sex allocation of a species) will necessarily play a key role in determining the fate of a new polyploid lineage. The effects of the sexual system on the evolution of polyploidy are complex and interactive. They include both aspects of the genetic system, the genetic load maintained in a population and the ecological context in which selection takes place. Here, we explore these complexities and review the empirical evidence for several potentially important genetic and ecological interactions between ploidy and the sexual system in plants. We place particular emphasis on work in our laboratory on the European annual plant Mercurialis annua , which offers promising scope for detailed investigations on this topic. M. annua forms a polyploid complex that varies in its sexual system from dioecy (separate sexes) through androdioecy (males and hermaphrodites) to functional hermaphroditism.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 547–560.     

Androdioecy and the evolution of dioecy

The likelihood that dioecy could evolve via androdioecy is examined. It is concluded that female-sterility mutations are unlikely to be able to invade populations of self-compatible hermaphrodite species, even if the resources that an hermaphrodite devotes to seed production can be diverted to yield increased survival and also to increase male fertility. These findings are in agreement with the great rarity of androdioecy. Claimed cases of androdioecy are reviewed. All of the species in question appear to be functionally dioecious, with females retaining substantial anther vestiges. It is argued that this morphological androdioecy is in no way indicative of a previous functionally androdioecious state. The details of the reproductive biology of many of these species seem rather to be consistent with their having evolved dioecy via gynodioecy.
The rarity of androdioecy, as a route to the evolution of dioecy, suggests that re-allocation of reproductive resources is unlikely to be the sole factor of importance, and supports an important role for inbreeding avoidance. The fact that females in some dioecious species retain anthers of substantial size, containing considerable quantities of pollen, gives further support to the view that male-sterility mutations can sometimes be favoured even when little or no resources are re-allocated to male functions. This is impossible without substantial selfing and inbreeding. It is therefore concluded that inbreeding avoidance is generally important in the evolution of dioecy, though reallocation of reproductive resources is also necessary.     

The evolution of gender specialization from dimorphic hermaphroditism: paths from heterodichogamy to gynodioecy and androdioecy

Several different pathways for the evolution of dioecy from hermaphroditism have been invoked and analyzed. These have largely considered either the spread of male- or female-sterility mutations in a monomorphic hermaphroditic population (i.e., the evolution of gynodioecy or androdioecy, respectively) or the gradual divergence in sex allocation of two classes of individuals, one that becomes increasingly male and the other that becomes increasingly female in functional gender (the paradioecy pathway). Here we assess the conditions under which male- or female-sterility mutations may invade and spread in a heterodichogamous population, that is, a dimorphic population composed of protandrous and protogynous individuals. Our model is formally applied to heterodichogamous populations, but the ideas we explore may also apply to the evolution of separate sexes in distylous species, where plants are either long- or short-styled. The model predicts that, under many circumstances, conditions for the evolution of gynodioecy and androdioecy in a heterodichogamous population are the same as those for their evolution from monomorphic populations. However, if one or the other of the two morphs are already somewhat specialized in their functional gender, as might occur if the quality or quantity of seed set is time dependent, the conditions for the invasion of males or females are relaxed. In particular, androdioecy can evolve more easily under such circumstances in heterodichogamous populations than in monomorphic hermaphroditic populations.     

Sexual dimorphism in intra- and interspecific competitive ability of the dioecious herb Mercurialis annua

Males and females of dioecious plant species often show different responses to competition with individuals of the same or opposite gender, but almost no data are available on the outcome of competition with members of other species. Here, we show that male and female individuals of the wind-pollinated herb Mercurialis annua are sexually dimorphic in both their intraspecific and interspecific competitive abilities. In a controlled experiment, we found that both sexes of M. annua were negatively affected by interspecific competition, but the sensitivity of males and females depended on the identity of their competitor species, with females tending to suppress the aboveground growth of competitor species more than males. Further, we found that intrasexual and intersexual competition affected the aboveground growth of males but not that of females: only males showed a significant reduction in growth when growing with conspecific competitors (male or female). We discuss our results with reference to related studies that suggest that males and females of M. annua have different resource requirements for reproduction, which in turn affect their competitive abilities.     

Density-dependent regulation of the sex ratio in an annual plant

Sex ratios are subject to strong frequency-dependent selection regulated by the mating system and the relative male versus female investment. In androdioecious plant populations, where males co-occur with hermaphrodites, the sex ratio depends on the rate of self-fertilization by hermaphrodites and on the relative pollen production of males versus hermaphrodites. Here, we report evolutionary changes in the sex ratio from experimental mating arrays of the androdioecious plant Mercurialis annua. We found that the progeny sex ratio depended strongly on density, with fewer males in the progeny of plants grown under low density. This occurred in part because of a plastic adjustment in pollen production by hermaphrodites, which produced more pollen when grown at low density than at high density. Our results provide support for the prediction that environmental conditions govern sex ratios through their effects on the relative fertility of unisexual versus hermaphrodite individuals.     

Two's company, three's a crowd: experimental evaluation of the evolutionary maintenance of trioecy in Mercurialis annua (Euphorbiaceae)

Trioecy is an uncommon sexual system in which males, females, and hermaphrodites co-occur as three clearly different gender classes. The evolutionary stability of trioecy is unclear, but would depend on factors such as hermaphroditic sex allocation and rates of outcrossing vs. selfing. Here, trioecious populations of Mercurialis annua are described for the first time. We examined the frequencies of females, males and hermaphrodites across ten natural populations and evaluated the association between the frequency of females and plant densities. Previous studies have shown that selfing rates in this species are density-dependent and are reduced in the presence of males, which produce substantially more pollen than hermaphrodites. Accordingly, we examined the evolutionary stability of trioecy using an experiment in which we (a) indirectly manipulated selfing rates by altering plant densities and the frequency of males in a fully factorial manner across 20 experimental plots and (b) examined the effect of these manipulations on the frequency of the three sex phenotypes in the next generation of plants. In the parental generation, we measured the seed and pollen allocations of hermaphrodites and compared them with allocations by unisexual plants. In natural populations, females occurred at higher frequencies in denser patches, a finding consistent with our expectations. Under our experimental conditions, however, no combination of plant densities and male frequencies was associated with increased frequencies of females. Our results suggest that the factors that regulate female frequencies in trioecious populations of M. annua are independent of those regulating male frequencies (density), and that the stable co-existence of all three sex phenotypes within populations is unlikely.     

Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems

A functional view of gender helps evolutionary biologists evaluate the mechanisms underlying breeding-system evolution. Evolutionary pathways from hermaphroditism to dioecy include the intermediate breeding systems of gynodioecy and androdioecy. These pathways start with the invasion of unisexual mutants, females or males, respectively, followed by alteration of the hermaphrodites to allocate more to the sexual function that the unisexuals lack. Eventually, hermaphrodites become unisexual and dioecy has evolved. Some species evolving along these pathways stop short of completing this second step, or even revert back from dioecy. We evaluate the hypothesis that gender plasticity is involved in these transitions to and from dioecy. Evidence from studies of subdioecious species that have evolved along the gynodioecy pathway suggests that gender plasticity occurs and stabilizes subdioecy by lowering the cost of producing seed. Factors influencing species evolving toward androdioecy, or reverting to androdioecy from dioecy, appear to be more varied and include reproductive assurance, herbivory and gender plasticity. In general, gender specialization appears to be favored in resource-poor environments regardless of which pathway is taken to dioecy.     

Functional dioecy in <Emphasis Type="Italic">Morinda parvifolia</Emphasis> (Rubiaceae), a species with stigma-height dimorphism

The evolution of dioecy from heterostyly has been well documented, but detailed studies on this transitional process are rare. Here we report the occurrence of cryptic dioecy in a perennial liana species with stigma-height dimorphism, Morinda parvifolia Bartl. ex DC. (Rubiaceae). Floral morphology, ancillary characters and cross compatibility of long-styled (L-morph) and short-styled (S-morph) were examined. L-morph and S-morph display obvious pistil dimorphisms, with the stigma of S-morph lacking papillae cells. Both floral morphs show similar pollen morphology, although pollen viability is higher in S-morph than in L-morph. S-morph flowers produce viable pollen grains but much reduced stigma and set no fruits, functioning as males; L-morphs, although with viable pollen grains and receptive stigmas, exhibit strong self- and intramorph incompatibility, with self- and intramorph pollen tubes arrested in the stigma lobes and the upper part of style, respectively, resulting in L-morphs functioning only as females. The species thus has physiological androdioecy but functional dioecy. This might be the first case showing the possibility that androdioecy could be a mid-stage in the pathway of dioecy evolving from stigma-height dimorphism.     

Low siring success of females with an acquired male function illustrates the legacy of sexual dimorphism in constraining the breakdown of dioecy

Dioecy has often broken down in flowering plants, yielding functional hermaphroditism. We reasoned that evolutionary transitions from dioecy to functional hermaphroditism must overcome an inertia of sexual dimorphism, because modified males or females will express the opposite sexual function for which their phenotypes have been optimised. We tested this prediction by assessing the siring success of monoecious individuals of the plant Mercurialis annua with an acquired male function but that are phenotypically still female‐like. We found that pollen dispersed by female‐like monoecious individuals was ~ 1/3 poorer at siring outcrossed offspring than pollen from monoecious individuals with an alternative male‐like inflorescence. We conclude that whereas dioecy might evolve from functional hermaphroditism by conferring upon individuals certain benefits of sexual specialisation, reversion from a strategy of separate sexes to one of combined sexes must overcome constraints imposed by the advantages of sexual dimorphism. The breakdown of dioecy must therefore often be limited to situations in which outcrossing cannot be maintained and where selection favours a capacity for inbreeding by functional hermaphrodites.     

Evolutionary transitions among dioecy,androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata)

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.     

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.     

Gender specialization in <Emphasis Type="Italic">Palicourea demissa</Emphasis> (Rubiaceae), a distylous,hummingbird-pollinated treelet

Distyly has been interpreted as a mechanism that promotes cross-pollination among conspecific plants and as one of the routes leading to the evolution of dioecy. In one of the possible evolutionary pathways, pollinators may disrupt intermorph pollen flow, and, as a consequence, floral morphs may gradually specialize as either male or female (functional dioecy). Natural patterns of pollen deposition and fruit and seed production were estimated in Palicourea demissa (Rubiaceae) and used as parameters to assess functional gender differences between floral morphs. Pollen flow was asymmetrical in P. demissa. Long-styled flowers were more effective than short-styled flowers in pollen deposition towards compatible stigmas, whereas short-styled flowers were more effective in legitimate pollen receipt. Accordingly, short-styled plants produced more fruits and viable seeds than long-styled plants. The contributions of male and female function to the potential functional gender were equivalent in both morphs. However, the realized functional gender deviated significantly from the potential functional gender in both morphs, in which short-styled plants were more successful through their female function, but long-styled plants through their male function. If pollinators disrupt the complementarities of pollen transfer between the two morphs (asymmetric pollen flow), the expression of a more profitable gender is expected in each morph. Thus, our results support the hypothesis that dioecy may evolve in distylous populations through the gradual specialization of each morph as either male or female.     

YEAR-TO-YEAR CHANGES IN PHENOTYPIC GENDER IN A MONOECIOUS CUCURBIT,APODANTHERA UNDULATA

Year-to-year variation in phenotypic gender in the monoecious cucurbit, Apodanthera undulata Gray was investigated. Small plants produce no flowers. Larger plants produce only staminate flowers (“male” plants), while a somewhat greater threshold size is necessary for pistillate flower production (cosexual plants). Approximately 85% of the plants that bloomed did not change gender group between years. Two measures of phenotypic gender were used: prospective femaleness, a measure standardized to the population floral ratio, and morphological femaleness, an unstandardized measure. Femaleness of cosexes between years was positively correlated; r values were somewhat greater when using morphological femaleness values. Plants that opened only staminate flowers one year were likely to open only staminate flowers the next year. Similarly, cosexes were likely to be cosexes again the following year, with similar femaleness values. Beyond the threshold size for pistillate flower production, plant size was not correlated with femaleness. These patterns suggest that all plants are male until they reach a certain size and that plants in their cosexual phase may have an intrinsic femaleness tendency due to either genotype or microsite effects.     

Density-dependent self-fertilization and male versus hermaphrodite siring success in an androdioecious plant

Models of mating-system evolution emphasize the importance of frequency-dependent interactions among mating partners. It is also known that outcross siring success and the selfing rate in self-compatible hermaphrodites can be density dependent. Here, we use array experiments to show that the mating system (i.e., the outcrossing rate) and the siring success of morphs with divergent sex allocation strategies are both density dependent and frequency dependent in androdioecious populations of the wind-pollinated, annual plant Mercurialis annua. In particular, the outcrossing rate is a decreasing function of the mean interplant distance, regulated by a negative exponential pollen fall-off curve. Our results indicate that pollen dispersed from a male inflorescence are over 60% more likely to sire outcrossed progeny than equivalent pollen dispersed from hermaphrodites, likely due to the fact that males, but not hermaphrodites, disperse their pollen from erect inflorescence stalks. Because of this difference, and because males of M. annua produce much more pollen than hermaphrodites, the presence of males in the experimental arrays reduced both the selfing rate and the outcross siring success of hermaphrodites. We use our results to infer a density threshold below which males are unable to persist with hermaphrodites but above which they can invade hermaphroditic populations. We discuss our findings in the context of a metapopulation model, in which males can only persist in well-established populations but are excluded from small, sparse populations, for example, in the early stages of colonization.