Multiple sex expressions in Cimicifuga simplex: dichogamy destabilizes hermaphroditism

Cimicifuga simplex (Ranunculaceae) has four types of individuals, differing in their sex expression: there are individuals with hermaphroditic, hermaphroditic and male (andromonoecious), only male, or only female flowers. Purely female individuals appear during the early part of the flowering period of the population, and males during the later part. Strong protandry in hermaphroditic flowers causes a shift in functional sex ratio in the population over time. This facilitates the evolution and maintenance of small proportions of unisexual individuals in the population. A hypothesis developed from this case of multiple sex expression predicts dichogamy as a near-universal feature of andro-and gynomonoecious, androdioecious, and gynodioecious species, and also specific temporal distributions for each sex form depending upon the form of dichogamy. Results of tests on large sets of species strongly support the relevance of this hypothesis.     

Dichogamy, Sex Allocation, and Mating System of Campanula microdonta and C. punctata

Dichogamy and sex allocation in several populations of Campanula microdonta and C. punctata were investigated with regard to their mating systems. Duration of the staminate phase differed among the populations: staminate phase was longer in self-compatible (SC) and largely outcrossing populations than in self-incompatible (SI) and outcrossing populations or in SC and largely inbreeding populations. Duration of the pistillate phase among the populations was less variable than duration of the staminate phase. Male reproductive effort decreased with increase of the estimated selfing rates. Male allocation (weight ratio of androecium to gynoecium or to total flower) may be used as an indicator of the breeding system. Within each population, small flowers allocate proportionately more resources to the androecium than to the gynoecium. Among populations, SC outcrossing populations tend to produce large ovaries, and SC inbreeding populations tend to produce small ovaries.     

Dichogamy,gender variation and bet-hedging inPseudowintera colorata

Summary Temporal patterns of variability in the longevity of the male and female phases of individual flowers and in the gender expression of plants of a dichogamous New Zealand tree,Pseudowintera colorata (Winteraceae), were documented in field studies. Two measures for the duration of phases in a dichogamous flower are distinguished; the nominal phases based on morphological features of the flower, and the effective phases reflecting the duration of their functions. Flower and phase longevity and phenotypic gender varied considerably throughout the season and among individuals. Temporal variability in phenotypic gender was loosely synchronized among the 12 plants sampled. Three effects of an environmental factor (temperature) were noted. First, increased temperatures shortened the duration of the female phase but had no effect on the duration of the male phase. Second, pollination frequency was positively correlated with temperature. These results indirectly suggest that increased pollination may shorten the duration of the female phase. Third, average population maleness, measured as the proportion of open flowers in the population on a given day which were in the male phase, was positively correlated with temperature. It is postulated that temperature indirectly influences temporal patterns of gender expression in the population through its differential effects on the longevity of the male and female phases in individual flowers. A theoretical model of bet-hedging shows that, if the direction of an environmental effect on the proportions of the sexual phases is irreversible, selection favours asynchronous dichogamy and reduces the temporal variability as much as possible. If the direction of the response is reversible, heterodichogamy is favoured.     

The differential contributions of herkogamy and dichogamy as mechanisms of avoiding self‐interference in four self‐incompatible Epimedium species

Self‐interference is one of the most important selective forces in shaping floral evolution. Herkogamy and dichogamy both can achieve reductions in the extent of self‐interference, but they may have different roles in minimizing self‐interference in a single species. We used four self‐incompatible Epimedium species to explore the roles of herkogamy and dichogamy in avoiding self‐interference and to test the hypothesis that herkogamy and dichogamy may be separated and become selected preferentially in the taxa. Two species (E. franchetii and E. mikinorii) expressed strong herkogamy and weak protogyny (adichogamy), whereas another two species (E. sutchuenense and E. leptorrhizum) expressed slight herkogamy and partial protandry. Field investigations indicated that there was no physical self‐interference between male function and female function regarding pollen removal and pollen deposition in all species. Self‐pollination (autonomous or facilitated) was greater in species with slight herkogamy than in those with strong herkogamy. Artificial pollination treatments revealed that self‐pollination could reduce outcrossed female fertility in all species, and we found evidence that self‐interference reduced seed set in E. sutchuenense and E. leptorrhizum in the field, but not in E. franchetii and E. mikinorii. These results indicate that well‐developed herkogamy is more effective compared with dichogamy in avoiding self‐interference in the four species. In genus Epimedium, herkogamy instead of dichogamy should be selected preferentially and evolved as an effective mechanism for avoiding self‐interference and might not need to evolve linked with dichogamy.     

Experimental analysis of protogyny in Aquilegia canadensis (Ranunculaceae)

Dichogamy is very common in flowering plants and is widely thought to reduce pollen-pistil interference, especially self-pollination. Yet, the functional significance of dichogamy has rarely been studied. We investigated the nature and functioning of dichogamy in eastern Ontario populations of Aquilegia canadensis, a highly selfing columbine previously described as protogynous. We then manipulated flowers to determine whether increased protogyny would reduce self-fertilization. Contrary to previous reports, A. canadensis is not dichogamous. Controlled pollinations in a greenhouse showed that pollen tubes generally begin to develop after anther dehiscence. Although stigmas can collect pollen early in floral development, naturally pollinated flowers collected from four populations had few pollen grains on stigmas and almost no pollen tubes in styles until after anther dehiscence. Limited pollen deposition before anther dehiscence was also associated with low nectar availability and limited sepal expansion. Because inbreeding depression is strong in this species, selection may favor increased protogyny if it reduces selfing. We tested this hypothesis by comparing the level of selfing in flowers rendered protogynous by the removal of the first 19 (of 39) anthers to develop, with nonprotogynous control flowers. Contrary to expectations, protogyny did not reduce selfing. Our results emphasize the importance of detailed field observations and manipulative experiments in understanding the nature and functional significance of dichogamy.     

On flower visitors and true pollinators: The case of protandrous Heracleum sphondylium L. (Apiaceae)

Hogweed (Heracleum sphondylium L.), a common European umbellifer, is very variable in terms of flower and inflorescence morphology. Its flowers are visited by numerous insects, yet little is known about the importance of the particular insect taxa. I observed umbels of two colour morphs (subspecies) of Heracleum sphondylium growing in NE Poland, which were visited by more than 108 insect species during two study seasons. Analysis of the insects' importance suggests that the most efficient pollinators are the medium-sized flies Eriozona syrphoides, and Lucilia spp. (Diptera). Bumblebees Bombus terrestris (Hymenoptera), beetles of genus Stenurella spp. and Dasytes spp. (Coleoptera) and flies Eristalis spp., Meliscaeva cinctella, Phaonia angelicae and Thricops nigrifrons also contribute to pollination of the studied plants, but their efficiency shows considerable seasonal variation. Although the dense umbels of the white flowered H. sphondylium subsp. sphondylium are generally more attractive for insect visitors than the loose yellowish inflorescences of H. sphondylium subsp. sibiricum, these taxa do not seem to attract different sets of the pollinators. For both subspecies, flowers in the staminate phase were visited significantly more often than those in the pistillate phase. Some flower visitors visited the staminate phase only, which suggests they may be parasites rather than pollinators.     

A model of the evolution of dichogamy incorporating sex-ratio selection, anther-stigma interference, and inbreeding depression

Historically, explanations for the evolution of floral traits that reduce self-fertilization have tended to focus on selection to avoid inbreeding depression. However, there is growing support for the hypothesis that such traits also play a role in promoting efficient pollen dispersal by reducing anther-stigma interference. The relative importance of these two selective pressures is currently a popular topic of investigation. To date, there has been no theoretical exploration of the relative contributions of selection to avoid the genetic costs of self-fertilization and selection to promote efficient pollen dispersal on the evolution of floral traits. We developed a population genetic model to examine the influence of these factors on the evolution of dichogamy: the temporal separation of anther maturation and stigma receptivity. Our analysis indicates that anther-stigma interference can favor dichogamy even in the absence of in-breeding depression. Although anther-stigma interference and inbreeding depression are the key forces driving the initial evolution of dichogamy, selection to match the timing of pollen dispersal to the availability of ovules at the population level becomes a more potent force opposing the further evolution of dichogamy as the extent of temporal separation increases. This result may help to explain otherwise puzzling phenomena such as why dichogamy is rarely complete in nature and why dichogamy tends to be associated with asynchronous flower presentation.     

Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees

Background and Aims

Pollen-collecting bees are among the most important pollinators globally, but are also the most common pollen thieves and can significantly reduce plant reproduction. The pollination efficiency of pollen collectors depends on the frequency of their visits to female(-phase) flowers, contact with stigmas and deposition of pollen of sufficient quantity and quality to fertilize ovules. Here we investigate the relative importance of these components, and the hypothesis that floral and inflorescence characteristics mediate the pollination role of pollen collection by bees.

Methods

For ten Aloe species that differ extensively in floral and inflorescence traits, we experimentally excluded potential bird pollinators to quantify the contributions of insect visitors to pollen removal, pollen deposition and seed production. We measured corolla width and depth to determine nectar accessibility, and the phenology of anther dehiscence and stigma receptivity to quantify herkogamy and dichogamy. Further, we compiled all published bird-exclusion studies of aloes, and compared insect pollination success with floral morphology.

Key Results

Species varied from exclusively insect pollinated, to exclusively bird pollinated but subject to extensive pollen theft by insects. Nectar inaccessibility and strong dichogamy inhibited pollination by pollen-collecting bees by discouraging visits to female-phase (i.e. pollenless) flowers. For species with large inflorescences of pollen-rich flowers, pollen collectors successfully deposited pollen, but of such low quality (probably self-pollen) that they made almost no contribution to seed set. Indeed, considering all published bird-exclusion studies (17 species in total), insect pollination efficiency varied significantly with floral shape.

Conclusions

Species-specific floral and inflorescence characteristics, especially nectar accessibility and dichogamy, control the efficiency of pollen-collecting bees as pollinators of aloes.     

Phenological match drives pollen‐mediated gene flow in a temporally dimorphic tree

• Variation in flowering phenology is common in natural populations, and is expected to be, together with inter‐mate distance, an important driver of effective pollen dispersal. In populations composed of plants with temporally separated sexual phases (i.e. dichogamous or heterodichogamous populations), pollen‐mediated gene flow is assumed to reflect phenological overlap between complementary sexual phases. In this study, we conducted paternity analyses to test this hypothesis in the temporally dimorphic tree Acer opalus.
• We performed spatially explicit analyses based on categorical and fractional paternity assignment, and included tree size, pair‐wise genetic relatedness and morph type as additional predictors. Because differences between morphs in flowering phenology may also influence pollination distances, we modelled separate pollen dispersal kernels for the two morphs.
• Extended phenological overlap between male and female phases (mainly associated with inter‐morph crosses) resulted in higher siring success after accounting for the effects of genetic relatedness, morph type and tree size, while reduced phenological overlap (mainly associated with intra‐morph crosses) resulted in longer pollination distances achieved. Siring success also increased in larger trees.
• Mating patterns could not be predicted by phenology alone. However, as heterogeneity in flowering phenology was the single morph‐specific predictor of siring success, it is expected to be key in maintaining the temporal dimorphism in A. opalus, by promoting not only a prevalent pattern of inter‐morph mating, but also long‐distance pollination resulting from intra‐morph mating events.