Disassortative mating, sexual specialization, and the evolution of gender dimorphism in heterodichogamous Acer opalus

In sexually polymorphic species, the morphs are maintained by frequency-dependent selection through disassortative mating. In heterodichogamous populations in which disassortative mating occurs between the protandrous and protogynous morphs, a decrease in female fitness in one morph is hypothesized to drive sexual specialization in the other morph, resulting in dimorphic populations. We test these ideas in a population of the heterodichogamous species, Acer opalus . We assessed both prospective gender of individuals in terms of their allocations and actual parentage using microsatellites; we found that most matings in A. opalus occur disassortatively. We demonstrate that the protogynous morph is maintained by frequency-dependent selection, but that maintenance of males versus protandrous individuals depends on their relative siring success, which changes yearly. Seeds produced later in the reproductive season were smaller than those produced earlier; this should compromise reproduction through ovules in protandrous individuals, rendering them male biased in gender. Time-dependent gender and paternity analyses indicate that the sexual morphs are specialized in their earlier sexual functions, mediated by the seasonal decrease in seed size. Our results confirm that mating patterns are context-dependent and change seasonally, suggesting that sexual specialization can be driven by seasonal effects on fitness gained through one of the two sexual functions.     

Sex expression in EgyptianThymelaea hirsuta (Thymelaeaceae) populations

The sex expression inThymelaea hirsuta was assessed in five habitats in the western Mediterranean desert of Egypt. The survey over two main flowering periods indicated that the sexual expression of this plant is complex and labile. Beside the dioecious male and female states, five monoecious states were detected. The dioecious states are more abundant and less labile. There is a clear shift from monoecious towards dioecious states and in general favour of males from the first (late autumn) to the second (late winter) flowering period. These results are discussed in view of the adaptive theories and evolution.     

Flowering phenology and mating success of the heterodichogamous tree Machilus thunbergii Sieb. et Zucc (Lauraceae)

Heterodichogamy is defined as the presence of two flower morphs that exhibit male and female functions at different times among individuals within a population, and is regarded as an adaptation to promote outbreeding through enhanced intermorph pollination. In highly fragmented populations in which the morph frequency is biased, heterodichogamy may hamper population growth by reducing seed sets of the more numerous morph, and enhancing seed sets of the less numerous morph. In such situations, we hypothesize that individual plants experience greater seed sets if the opposite sexual morphs are nearby, and that individuals of a less numerous sexual morph have greater seed sets. After confirming heterodichogamy by observing flowering behavior and phenology, we tested these two hypotheses in a highly fragmented population of Machilus thunbergii, a putative heterodichogamous evergreen laurel tree. Our observations confirmed that M. thunbergii is heterodichogamous, consisting of two types of protogynous and bisexual flowers: a morning female (MF)–afternoon male morph and a morning male (MM)–afternoon female morph at the individual level. Sexual expression of the two morphs was highly synchronized and reciprocal. Investigation of seed‐set rates revealed greater rates of both morphs if the opposite morph was nearby. The less numerous sexual morph (MF) showed a greater seed‐set rate than the more numerous sexual morph (MM).     

Disassortative mating and the maintenance of sexual polymorphism in painted maple

Since Darwin's pioneering research on plant reproductive biology (e.g. Darwin 1877), understanding the mechanisms maintaining the diverse sexual strategies of plants has remained an important challenge for evolutionary biologists. In some species, populations are sexually polymorphic and contain two or more mating morphs (sex phenotypes). Differences in morphology or phenology among the morphs influence patterns of non-random mating. In these populations, negative frequency-dependent selection arising from disassortative (intermorph) mating is usually required for the evolutionary maintenance of sexual polymorphism, but few studies have demonstrated the required patterns of non-random mating. In the current issue of Molecular Ecology, Shang et al. (2012) make an important contribution to our understanding of how disassortative mating influences sex phenotype ratios in Acer pictum subsp. mono (painted maple), a heterodichogamous, deciduous tree of eastern China. They monitored sex expression in 97 adults and used paternity analysis of open-pollinated seed to examine disassortative mating among three sex phenotypes. Using a deterministic 'pollen transfer' model, Shang et al. present convincing evidence that differences in the degree of disassortative mating in progeny arrays of the sex phenotypes can explain their uneven frequencies in the adult population. This study provides a useful example of how the deployment of genetic markers, demographic monitoring and modelling can be integrated to investigate the maintenance of sexual diversity in plants.     

Gender specialization and factors affecting fruit set of the wind-pollinated heterodichogamous Juglans regia

Gender expression, flowering phenology, reproductive performance and factors affecting fruit set (i.e., flowering synchrony, size and distance to the nearest pollen donor) were investigated in a cultivated population of a wind-pollinated self-compatible heterodichogamous Juglans regia (Juglandaceae). Four flowering morphs, (i.e., protandrous, protogynous, male and female) were observed. The sexual functions of the protandrous and protogynous morphs were almost synchronous; however, they were not reciprocal, and the separation of male and female flowering within most monoecious individuals was not complete. Thus, within-morph mating and geitonogamous pollination may be common. The ratio of protandrous versus protogynous morphs was biased towards the protandrous morph, but the fruit set did not differ between the morphs, suggesting that the fruit set of the protandrous morph could be partly compensated by within-morph pollination. The ratio of the female flower number or fruit number to the total male catkin length was higher in the protogynous morph than in the protandrous morph and did not vary with plant size, suggesting that gender variation was not size dependent and that the sexual function of protandrous morphs was more male biased. Fruit set depended on plant size only for protandrous morphs. The fruit set of individual plants decreased with increasing distance to the nearest pollen donor regardless of morph, possibly because of pollen limitation. The fruit set of individual plants increased with flowering synchrony, indicating that flowering synchrony could affect reproductive success.     

Repeated evolution of dioecy from androdioecy in Acer

The evolution of breeding systems was studied in the genus Acer, with special attention to the origin of androdioecy and dioecy, using a phylogenetic approach. Parsimony and maximum-likelihood techniques were used to infer the ancestral character state and trends in the evolution of breeding systems. Information on breeding systems was obtained from the literature, and phylogenetic relationships were taken from three published phylogenies. Although a general trend from duodichogamy to dioecy through heterodichogamy has been proposed for the genus Acer, our results show that a general trend is not detected when phylogenetic relationships are taken into account. Dioecy appeared as a derived state that evolved at least three times and never reversed towards other states. Three different paths to dioecy have been followed in the genus Acer: from heterodichogamous androdioecy; from heterodichogamous trioecy; and from dichogamous subdioecy. Therefore, although the best documented cases of evolution of androdioecy indicate that this breeding system evolves from dioecy, in the genus Acer the opposite situation occurs (androdioecy leading to dioecy). Here we discuss the role of inbreeding avoidance and sexual specialization as selective forces driving the evolution of dioecy in the genus Acer.     

Inflorescence dimorphism,heterodichogamy and thrips pollination in Platycarya strobilacea (Juglandaceae)

Background and Aims

Unlike other taxa in Juglandaceae or in closely related families, which are anemophilous, Platycarya strobilacea has been suggested to be entomophilous. In Juglandaceae, Juglans and Carya show heterodichogamy, a reproductive strategy in which two morphs coexist in a population and undergo synchronous reciprocal sex changes. However, there has been no study focusing on heterodichogamy in the other six or seven genera, including Platycarya.

Methods

Inflorescence architecture, sexual expression and pollination biology were examined in a P. strobilacea population in Japan. Flowering phenology was monitored daily for 24 trees in 2008 and 27 in 2009. Flower visitors and inhabitants were recorded or collected from different sexes and stages.

Key results

The population of P. strobilacea showed heterodichogamous phenology with protogynous and duodichogamous–protandrous morphs. This dimorphism in dichogamy was associated with distinct inflorescence morphologies. Thrips pollination was suggested by the frequent presence of thrips with attached pollen grains, the scarcity of other insect visitors, the synchronicity of thrips number in male spikes with the maturation of female flowers, and morphological characters shared with previously reported thrips-pollinated plants. Male spikes went through two consecutive stages: bright yellow and strong-scented M1 stage, and brownish and little-scented M2 stage. The latter contained more thrips, synchronized better with the receptive stage of female flowers of the reciprocal morph and is probably the main period of pollen export.

Conclusions Platycarya strobilacea

is heterodichogamous and thrips-pollinated, both of which are relatively rare conditions in angiosperms. In male spikes of P. strobilacea, there is probably a temporal decoupling of pollinator attraction and pollen export.     

Adaptive significance of flexistyly in Alpinia blepharocalyx (Zingiberaceae): a hand-pollination experiment

BACKGROUND AND AIMS: Flexistyly is a sexual dimorphism where there are two morphs that differ in the temporal expression of sexual function and also involve reciprocal movement of the stigmatic surface through a vertical axis during the flowering period. The adaptive significance of flexistyly has been interpreted as a floral mechanism for outcrossing, but it may also function to reduce sexual interference in which styles and stigmas impede the pollen export. Here these two explanations of flexistyly were tested in Alpinia blepharocalyx through a hand-pollination experiment. METHODS: Hand-pollinations were performed in two temporal morphs and consisted of two sequential pollination treatments, namely self-pollination in the morning and inter-morph pollination in the afternoon (treatment 1) or conversely inter-morph pollination in the morning and self-pollination in the afternoon (treatment 2), and two simultaneous self- and inter-morph cross-pollination treatments either in the morning (treatment 3) or in the afternoon (treatment 4). Seed paternity was then determined to assess relative success of self- versus cross-pollen using allozyme markers. KEY RESULTS: In the sequential pollination treatments, whether the stigmas of recipients are receptive in the morning is crucial to the success of the pollen deposited. When the cataflexistylous (protandrous) morph served as pollen recipient, early-arriving pollen in the morning can sire only a very small proportion (<15%) of seeds because the stigmas were then unreceptive. However, when the anaflexistylous (protogynous) morph served as pollen recipient, early pollen did gain a large competitive advantage over the late pollen, particularly when cross-pollen arrived first. Simultaneous self- and inter-morph cross-pollination indicated that outcross-pollen is more competitive than self-pollen on receptive stigmas. CONCLUSIONS: Differential maturing of male and female organs in Alpinia blepharocalyx is sufficient for selfing avoidance, obviating the need for style movements. Instead, the upward style curvature of the cataflexistylous morph in the morning and the anaflexistylous morph in the afternoon most likely represents a means of reducing interference with pollen export.     

Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae)

Mating patterns in heterodichogamous species are generally considered to be disassortative between flowering morphs, but this hypothesis has hitherto not been vigorously tested. Here, mating patterns and pollen dispersal were studied in Juglans mandshurica, a heterodichogamous wind-pollinated species that is widely distributed in northern and north-eastern China. Paternity analyses carried out on 11 microsatellite loci were used to estimate morph-specific rates of outcrossing and disassortative mating. Pollen dispersal and genetic structure were also investigated in the population under study. The mating pattern of J. mandshurica was highly outcrossing and disassortative. Pairwise values of intramorph relatedness were much higher than those of intermorph relatedness, and a low level of biparental inbreeding was detected. There was no significant difference in outcrossing and disassortative mating rates between the two morphs. The effective pollen dispersal distribution showed an excess of near-neighbor matings, and most offspring of individual trees were sired by one or two nearby trees. These results corroborate the previous suggestion that mating in heterodichogamous plant species is mainly disassortative between morphs, which not only prevents selfing but also effectively reduces intramorph inbreeding.