The maintenance of gynodioecy and androdioecy in angiosperms

Algebraic models of gynodioecy show that the effects on the equilibrium sex ratio of the relative survival and seed production of the sexes and of inbreeding of male-fertile plants are identical for all genic modes of inheritance, provided that different genotypes among male-fertile plants (or among females) do not differ in average fitness. The effects of three modes of inbreeding on equilibrium sex ratios are examined. If there is competition between self- and cross-fertilization of male-fertile individuals, a stable sexual dimorphism can be maintained by an outbreeding advantage of females if both the proportion of cross-fertilized seeds among those borne on male-fertile individuals,t, and the inbreeding depression (fitness inbred/outbred seeds),i, are less than one half. A lower frequency of females is obtained for the same values oft andi if self-fertilization precedes cross-fertilization. If self-fertilization follows cross-fertilization, gynodioecy cannot be maintained by an outbreeding advantage of females. When the sex phenotypes of gynodioecious populations are determined by cytoplasmic inheritance, females need only a slight advantage over males in survival, ovule production or outbreeding to persist at equilibrium. When determined by nuclear genes, androdioecy can be maintained by greater fecundity or a higher survival rate of males than of female-fertile plants, but not by an outbreeding advantage. Androdioecy cannot be maintained with cytoplasmic inheritance of sex. The models suggest explanations for the more frequent occurrence of gynodioecy than of andrdioecy, the high frequency of gynodioecy in Hawaii and New Zealand, and the origin of gynodioecy from hermaphrodite but not from monoecious ancestors.     

When males and hermaphrodites coexist: a review of androdioecy in animals

Androdioecy (populations consisting of males and hermaphrodites)is a rare mating system in plants and animals: up to 50 plantsand only 36 animals have been described as being androdioecious,with most of the latter being crustaceans. To date, a thoroughcomparative analysis of androdioecy in animals has not beenundertaken. Herein we present such an analysis. Androdioecyhas only been extensively surveyed in 2 animal taxa: the nematodeCaenorhabditis and the clam shrimp Eulimnadia. The other majortaxon having androdioecious species is the Cirripedia (barnacles),but there are only limited studies on androdioecy in this group.In animals, androdioecy is found either in species that havemorphologically and ecologically distinct sexes (that is, hermaphroditesand small, "complemental" males) that are derived from hermaphroditicancestors (that is, the barnacles) or in species that have similarly-sizedmales and hermaphrodites that have been derived from dioeciousancestors (the remaining androdioecious species). We suggestthat the barnacles have evolved a sexual specialization in theform of these complemental males that can more efficiently usethe constrained habitats that these barnacles often experience.For the remaining species, we suggest that androdioecy has evolvedas a response to reproductive assurance in species that experienceepisodic low densities. Additionally, we hypothesize that thedevelopment of mechanisms allowing reproductive assurance inspecies with a number of sexually differentiated traits is mostlikely to result in androdioecy rather than gynodioecy (mixturesof females and hermaphrodites), and that these species may bedevelopmentally constrained to stay androdioecious rather thanbeing capable of evolving into populations solely consistingof efficient, self-compatible hermaphrodites. We conclude bysuggesting several areas in need of further study to understandmore completely the evolution and distribution of this interestingmating system in animals.     

Do environmental factors affect the male frequency of exotic mangrove species <Emphasis Type="Italic">Laguncularia racemosa</Emphasis> (Combretaceae) along the southeast coast of China?

The exotic mangrove species Laguncularia racemosa (Combretaceae) is fast-growing and was used for forestation in recent years along the southeast coast of China. The breeding system of L. racemosa is variable among populations, such as hermaphroditism, gynodioecy, and androdioecy. To determine whether androdioecy is widespread in L. racemosa, 19 planted populations were surveyed along the southeast coast of China. To determine whether local environmental factors could affect the sex ratio in androdioecious populations, the observed male frequency of different populations was compared to local average annual temperature, rainfall, and salinity. The results showed that the 19 L. racemosa populations along the southeast coast of China were androdioecious. The male frequencies of these populations varied from 31.0 to ?88.9%. Partial correlation analysis showed that average annual salinity explained 74.7% of the male frequency (p?=?0.001). It is reasonable to note that the male frequency followed a general trend, presenting peak that coincided with the low salinity. The average annual rainfall explained only 30.4% of the male frequency (p?=?0.403). And the average annual temperature explained only 20.2% of the male frequency (p?=?0.206). The variable male frequency in different androdioecious L. racemosa populations may presumably be caused by ecological or genetical processes; these hypotheses will be tested in future studies.     

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.     

Breeding systems in the clam shrimp family Limnadiidae (Branchiopoda, Spinicaudata)

Abstract. Crustaceans in the class Branchiopoda exhibit a wide range of breeding systems, including dioecy (gonochorism), androdioecy, parthenogenesis, cyclic parthenogenesis, and hermaphroditism. The largest subgroup of the Branchiopods, the Diplostraca, is reported to encompass all five of these breeding systems. However, many of these reports are based primarily on simple observations of sex ratios in natural populations. Herein we report the beginnings of a more rigorous approach to breeding system determination in the Diplostraca, starting with the family Limnadiidae. We combine measurements of sex ratio, offspring rearings, and behavior to identify three breeding systems within the Limnadiidae: dioecy, androdioecy, and selfing hermaphroditism. To date, no instances of parthenogenetic reproduction have been identified in this family. Comparisons of breeding system determination via simple population sex ratios with our more controlled studies show that simple sex ratios can be useful when these sex ratios are ∼50% males (=dioecy) or 5–30% males (androdioecy). However, population sex ratios of 0–5% males or 35–45% males necessitate further investigation because estimates in these ranges cannot distinguish selfing hermaphroditism from androdioecy or androdioecy from dioecy, respectively. We conclude by noting that the genetic sex-determining system outlined for one of these limnadiid species, Eulimnadia texana , provides a parsimonious framework to describe the evolution of the three breeding systems observed within the Limnadiidae.     

Evolution of outcrossing in experimental populations of Caenorhabditis elegans

Caenorhabditis elegans can reproduce exclusively by self-fertilization. Yet, males can be maintained in laboratory populations, a phenomenon that continues to puzzle biologists. In this study we evaluated the role of males in facilitating adaptation to novel environments. For this, we contrasted the evolution of a fitness component exclusive to outcrossing in experimental populations of different mating systems. We introgressed a modifier of outcrossing into a hybrid population derived from several wild isolates to transform the wild-type androdioecious mating system into a dioecious mating system. By genotyping 375 single-nucleotide polymorphisms we show that the two populations had similar standing genetic diversity available for adaptation, despite the occurrence of selection during their derivation. We then performed replicated experimental evolution under the two mating systems from starting conditions of either high or low levels of diversity, under defined environmental conditions of discrete non-overlapping generations, constant density at high population sizes (N = 10⁴), no obvious spatial structure and abundant food resources. During 100 generations measurements of sex ratios and male competitive performance showed: 1) adaptation to the novel environment; 2) directional selection on male frequency under androdioecy; 3) optimal outcrossing rates of 0.5 under androdioecy; 4) the existence of initial inbreeding depression; and finally 5) that the strength of directional selection on male competitive performance does not depend on male frequencies. Taken together, these results suggest that androdioecious males are maintained at intermediate frequencies because outcrossing is adaptive.     

INBREEDING DEPRESSION IN ANDRODIOECIOUS POPULATIONS OF DATISCA GLOMERATA (DATISCACEAE)

Several workers have suggested that the rarity of androdioecy (the presence of males and hermaphrodites in a breeding population) in nature is due to the large fitness gain required by male plants in order to be maintained by selection. As part of an ongoing investigation of this hypothesis, we tested the effects of selfing on fitness in functionally androdioecious populations of Datisca glomerata. We compared progeny from self-fertilizations, cross-fertilizations with pollen from male plants only, cross-fertilizations with pollen from hermaphrodite plants only, and open-pollinated flowers for several measures of progeny fitness including seed weight, germination rate, and seedling weight. Significant inbreeding depression was observed for androdioecious populations of D. glomerata for both seed and seedling weights. However, no significant differences were observed across treatments for seed germination percentages. The observation of significant levels of inbreeding depression in this study, combined with prior evidence of threefold greater pollen production by males, may at least partially account for the large fitness increase required by males to be maintained by selection.     

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.     

Complex determination of male sterility in Thymus vulgaris L.: genetic and molecular analysis

Summary Nucleocytoplasmic determination of male sterility in Thymus vulgaris L. has been assumed in all papers attempting to explain the remarkably high frequencies of male steriles found in natural populations of this species. This paper provides strong evidence that both nuclear and cytoplasmic genes are involved in the determination of male sterility of this species, giving a complex inheritance. Interpopulation and intrapopulation crosses have shown that the ratio of females versus hermaphrodites among offsprings varied widely from 10 to 11. Furthermore, interpopulation crosses consistently yielded a higher frequency of females than intrapopulation crosses. Nucleocytoplasmic inheritance was demonstrated by an absence of male fertiles in backcrosses and asymmetrical segregation in reciprocal crosses. Molecular analysis of the mitochondrial DNA of some of the parents used in crosses suggested the involvement of different cytoplasms in the inheritance of male steriliy.     

Widespread functional android in Mercurialis annua L. (Euphorbiaceae)

The widespread coexistence of male and monoecious (cosexual) plants in Spanish, Portuguese and Moroccan populations of Mercurialis annua , an annual wind-pollinated ruderal, represents an important case of functional androdioecy, a rare breeding system in plants and animals. In M. annua , both males and cosexes disperse fully competent pollen. Quantitative gender varies discontinuously between males and cosexes, with males producing a mean of 6.09 times as much pollen as cosexes. It appears that gender is determined by a simple developmental switch, with male and cosexual inflorescences differing markedly in morphology: staminate flowers are borne on erect peduncles in males and in tight spiral clusters around a subsessile pistillate flower in cosexes. Males do not differ from cosexes in their biomass, but they are significantly taller, principally as a result of their greater internode lengths. The cosexual inflorescence is strongly protogynous so that outcrossing is favoured in dense stands, but seed-set is assured in cosexes isolated from prospective mates because of their ability to self-fertilize. Males typically occur at frequencies of less than about 30% in androdioecious populations, in accordance with theoretical predictions for functional androdioecy. In the genus Mercurialis , dioecy is the ancestral condition and monoecy and androdioecy, which occur in polyploid populations of M. annua , are derived. I argue here that androdioecy is most likely to evolve in plants (1) from dioecy, (2) in wind-pollinated species, and (3) in species with a colonizing habit. These predictions are also consistent with the limited published data available for other species.     

Selection in plant populations of effectively infinite size. V. Biallelic models of trioecy

A one-locus two-allele model of trioecy (presence of hermaphrodites, males and females in one population) is considered, in order to study the conditions for the persistence of this system. All possible assignments of the three sex types to the three genotypes are considered. This leads to three different modes of inheritance of trioecy, namely (a) females heterozygous, (b) males heterozygous and (c) hermaphrodites heterozygous, where in each mode each of the remaining two sex types is homozygous for one of the alleles. For mode (c) trioecy is always persistent, and the dependence of the sex ratio (for the three sex types) on the ovule and pollen fertilities and on the hermaphrodite selfing rate is specified. For the other two modes, (a) and (b), trioecy is not protected, i.e., it may not persist for any fertilities, viabilities or selfing rates. Thus, in this situation it is important to study the conditions under which the "marginal" systems of sexuality of trioecy, i.e., hermaphroditism, dioecy and gynodioecy in mode (a), and hermaphroditism, dioecy and androdioecy in mode (b), may become established. The results show that each marginal system may evolve from each other via trioecy. The evolution of dioecy is easier in mode (a) than in (b), so that female heterogamety would be expected to occur more often than male heterogamety in the present model. Under some conditions the breeding system obtained in equilibrium populations may depend on the initial genotype frequencies.—The necessity of considering modes of inheritance for sexual polymorphisms is demonstrated by comparing our results with those obtained from an evolutionary stable strategy (ESS) analysis of a purely phenotypic model.     

Ancient androdioecy in the freshwater crustacean Eulimnadia

Among the variety of reproductive mechanisms exhibited by living systems, one permutation--androdioecy (mixtures of males and hermaphrodites)--is distinguished by its rarity. Models of mating system evolution predict that androdioecy should be a brief stage between hermaphroditism and dioecy (separate males and females), or vice versa. Herein we report evidence of widespread and ancient androdioecy in crustaceans in the genus Eulimnadia, based on observations of over 33,000 shrimp from 36 locations from every continent except Antarctica. Using phylogenetic, biogeographical and palaeontological evidence, we infer that androdioecy in Eulimnadia has persisted for 24-180 million years and has been maintained through multiple speciation events. These results suggest that androdioecy is a highly successful aspect of the life history of these freshwater crustaceans, and has persisted for orders of magnitude longer than predicted by current models of this rare breeding system.     

Patterns of flowering and sex-ratio variation in the Mediterranean shrub Phillyrea angustifolia (Oleaceae): implications for the maintenance of males with hermaphrodites

The Mediterranean shrub Phillyrea angustifolia is one of the few plants that display androdioecy, a rare breeding system in which males co-occur with hermaphrodites. However, it has been difficult to account for male frequencies previously documented for this species, which have frequently been higher than 0.5. Here we present sex-ratio data from 13 sites in Spain and Portugal that throw further light on the maintenance of androdioecy in P. angustifolia . The inferred proportion of males in these populations was around 0.3, substantially lower that 0.5 and concurring with theoretical predictions for androdioecy. Differences in the proportion of hermaphrodites in flower between "stressed" and "nonstressed" sites suggest the existence of an important life-history trade-off between fruit production and the rate at which plants recover from recurrent disturbances such as fire. The reduced frequency of flowering by hermaphrodites relative to males may help to explain the maintenance of androdioecy in this long-lived, woody species.     

Physiologic,morphologic and behavioral responses of perpetual cultures ofCaulobacter crescentus to carbon,nitrogen and phosphorus limitations

Perpetual cultures ofCaulobacter crescentus were maintained in a chemostat and provided with media that provided glucose, glutamate, ammonium chloride, and Na/K phosphate as sources, respectively, of C, of C and N, of N and of P. All cultures were maintained at the same relative flow rate, f/V, so that reproductive rate was constant. As the CNP ratio was shifted from a balanced ratio of 100 g C9–10 g N1 g P, the cells modulated their rates of uptake, reducing the rates of uptake of excess element-sources and accelerating the uptake of potential sources of the limiting element. The change in N-limited cells was the greatest, resulting in a nearly 150-fold increase in rate of uptake of amino acids. Poly--hydroxybutyrate or polyphosphate was stored whenever C or P, respectively, was not the limiting element. Direct measurement of cell and stalk surface areas on purified peptidoglycan sacculi of P-limited cells revealed that the surface of both swarmer and stalked cells, as well as the stalk surface, participated in the accelerated rate of phosphate uptake. Swarmers from N-limited populations were the only cells that exhibited chemotactic responsiveness-to methionine, NH₄Cl and glutamate, but not to glucose or phosphate-sufficient to be detectable in a microcapillary assay. In populations that were C-limited and provided with ammonium ions as the principal source of N, morphogenesis and reproduction deteriorated and a steady state could not be maintained. Generally, the responses ofC. crescentus were appropriate to manage unbalanced nutrient supplies, but this oligoheterotrophic organism did not tolerate excesses of inorganic nutrients when limited for its sources of C, of energy, and of ammonium acceptor.     

Sex determination in the androdioecious barnacle Scalpellum scalpellum (Crustacea: Cirripedia)

How androdioecy (coexistence of hermaphrodites and males) is maintained is still poorly understood. Therefore, sex determination was studied in the androdioecious barnacle Scalpellum scalpellum L. First, 247 cypris larvae from seven broods were investigated for sexual dimorphism in larval morphology and found to be all identical. Second, experiments with cyprids showed that males and hermaphrodites differ distinctly in morphology as soon as 4–5 days after settlement. Third, 14 252 cyprids were allowed to settle on the bottom of their culture cages, and all surviving larvae developed into hermaphrodites and none into dwarf males. Fourth, larvae settled in hermaphrodite receptacles (i.e. future males) were removed at increasing intervals after settlement to study if the male and hermaphrodite sexual expressions are fixed or plastic. All larvae became dwarf males if allowed to stay there for more than 8 h after settlement. But if removed within 3 h after settlement, half of them developed into hermaphrodites. We conclude that an environmental sex determination mechanism operates in S. scalpellum. Together with a 1:1 hermaphrodite/male ratio observed in previously reported experiments offering a free choice of settlement, we suggest that all larvae are potential hermaphrodites, but only 50% can settle in hermaphrodite receptacles and yield males.     

Evolution de la constitution chimique elementaire de Pontella mediterranea au cours des dernieres generations annuelles dans le golfe de Marseille

Elementary chemical composition in carbon, hydrogen and nitrogenof the Pontellid Copepod Pontella mediterranea was studied on148 males and 146 females from automnal populations of the gulfof Marseilles, which are the last annual generations. Data arecompared to those obtained from spring and summer. The increasein animal weight from the last generations is greater in femalesthan males. The dry weight ratio of females against males is1.6 while it is only 1.4 in the previous generations. At theend of the natural biological cycle, C:N ratio shows a lightbut significant difference between males and females. The valuesof C:N ratio remain close to 3.4, which means that the observedincrease of animal weight on the last generations mainly proceedsfrom an increase in protein compounds.     

Mating behavior and time budget of an androdioecious crustacean,Eulimnadia texana (Crustacea: Conchostraca)

The clam shrimp,Eulimnadia texana (Crustacea, Conchostraca), is found in freshwater ephemeral environments throughtout the United States. Individual clam shrimp of this species are either hermaphroditic or male, a relatively rare mating system for animals known as androdioecy. Comparison of sex ratios between four neighboring populations ofE. texana in Southern New Mexico showed wide variation in the ratio of males to hermaphrodites with males making up as much as 42% of some populations and not occurring at all within others. Since little is known about the behavior of this species, an ethogram and time budget were prepared based on observations of laboratory populations. Males attempt to clasp hermaphrodites prior to mating. Precopulatory mate guarding occurs in this species. Outcrossing generally occurs during mate guarding and after the hermaphrodite molts. Hermaphrodites, however, seem to control the mating process. Successful mating by males never occured if the hermaphrodite struggled with him; hermaphrodite will self in the presence of males.     

Sperm dysfunction in sex ratio males of Drosophila subobscura

Drosophila subobscura has 128 spermatids per cyst, enclosed by two cyst cells. At beginning of elongation in control males the spermatid nuclei surround the head cyst cell nucleus, in sex ratio males nuclei are found throughout the cyst. Spermatid nuclei can elongate in any position in the cyst. Nuclei can be eliminated during individualization or degenerate after individualization. The number of sperm in any wrong position in the cyst varies in control males from 0 to about ten, in sex ratio males from 0 to more than 50. Two cyst sizes are distinguishable. At beginning of elongation small cysts have homogeneously stained spherical nuclei which later on are rod like. Large cysts have granulated nuclei which at first become spindle shaped and then slender. The length of the DNA containing part of elongated sperm heads of the long class is about 33 m in sex ratio and control males. The small sperm heads are 15 m in sex ratio but 20 m in control males. The complete DNA-containing-sperm-length is about 10% less in short sperm and 5% less in long sperm of sex ratio males than in those of control. Sex ratio males have more cysts per testis than control males. In sex ratio we counted 53.8%, in control males 49.4% short cysts.The work was supported by the grants N.S.F. GB-43209 and NIH GM 21732 and the Schweizerischer Nationalfonds zur Foerderung der wissenschaftlichen Forschung grant Nr. 3.815.72.     

Sex determination of the onion fly,Hylemya antiqua (Meigen)

In testes of many XXY₂ and XXY₂Y₂ males of Hylemya antiqua a numerical variation for Y₂, a consequence of mitotic nondisjunction, has been established. In 22 of 79 progenies of XXY₂ (including some unidentified XXY₂Y₂) males the ratio of females to males was significantly (p<0.05) different from 11, 9 with excess females and 13 with excess males. It could be concluded, firstly, that in progenies of XXY₂ males sex ratio distortion results from a numerical variation of Y₂ between the primordial germ cells of the male parent and secondly, that probably at least three primordial germ cells are involved in the formation of the male germ cells of the onion fly. Besides, the occurrence of some highly distorted sex ratios in male direction could be attributed to the presence of XXY₂Y₂ males. The frequency of M II cells with 2 Y₂ chromosomes established in XXY₂ males amounted to 2.9%. In XXY₂Y₂ males this percentage was higher and occasionally M IIs with 3 Y₂ were found. In the progeny of one cross a chromosome morphologically identical with Y₂ but lacking its holandric inheritance was found. From its inheritance, it could be concluded that it was a nonfunctional (mutated) Y₂ chromosome (Y_m). Interesting phenomena were the reduced transmission of Y_m through the female, and the observation of very high numbers of Y_m in some ovarian cells. A possible causal relationship between these two phenomena is discussed.     

Genetic variation and covariation among life history traits in populations of Acanthoscelides obtectus maintained on different hosts

We explored the extent to which two populations of Acanthoscelides obtectus (Coleoptera: Bruchidae), maintained in the laboratory for about 60 generations on common bean (Phaseolus vulgaris) and chickpea (Cicer arietinum) seeds, differ genetically in life history traits. Using a half-sib breeding design, we screened for genetic variation in oviposition preference for two hosts within both populations, and examined whether this variation is correlated with weevil pre-adult (egg-to-adult viability and egg-to-adult developmental time) and adult (female fecundity and longevity) fitness components on these two hosts. Significant differences between the Phaseolus and Cicer population were detected in viability, developmental time and oviposition preference, but not in female fecundity and longevity. The absence of a significant population × host interaction in all traits, except for developmental time in males, indicates that the Cicer population has not attained the status of host race. The estimated narrow-sense heritabilities within population within host plant were in the low-to-moderate level (range: 1%–79%), with an overall average of about 24%. Within the population maintained on the chickpeas we detected significant genetic correlations between female developmental time on chickpea seeds and preference for chickpeas. In the population maintained on the primary host of this weevil species (the Phaseolus population) we found no significant preference/performance genetic correlations. Data are also presented on the genetic correlations of preference and performance across host seeds within both populations. These correlations are found to be positive for all traits in both populations, indicating the absence of trade-offs in either performance or behavioural response that might impose selection for host specialization within populations.