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1.  Variation and evolution of herkogamy in Exochaenium (Gentianaceae): implications for the evolution of distyly 
Annals of Botany  2013;112(1):95-102.
Backgrounds and Aims
The spatial separation of stigmas and anthers (herkogamy) in flowering plants functions to reduce self-pollination and avoid interference between pollen dispersal and receipt. Little is known about the evolutionary relationships among the three main forms of herkogamy – approach, reverse and reciprocal herkogamy (distyly) – or about transitions to and from a non-herkogamous condition. This problem was examined in Exochaenium (Gentianaceae), a genus of African herbs that exhibits considerable variation in floral morphology, including the three forms of herkogamy.
Methods
Using maximum parsimony and maximum likelihood methods, the evolutionary history of herkogamic and non-herkogamic conditions was reconstructed from a molecular phylogeny of 15 species of Exochaenium and four outgroup taxa, based on three chloroplast regions, the nuclear ribosomal internal transcribed spacer (ITS1 and 2) and the 5·8S gene. Ancestral character states were determined and the reconstructions were used to evaluate competing models for the origin of reciprocal herkogamy.
Key results
Reciprocal herkogamy originated once in Exochaenium from an ancestor with approach herkogamy. Reverse herkogamy and the non-herkogamic condition homostyly were derived from heterostyly. Distylous species possessed pendent, slightly zygomorphic flowers, and the single transition to reverse herkogamy was associated with the hawkmoth pollination syndrome. Reductions in flower size characterized three of four independent transitions from reciprocal herkogamy to homostyly.
Conclusions
The results support Lloyd and Webb's model in which distyly originated from an ancestor with approach herkogamy. They also demonstrate the lability of sex organ deployment and implicate pollinators, or their absence, as playing an important role in driving transitions among herkogamic and non-herkogamic conditions.
doi:10.1093/aob/mct097
PMCID: PMC3690988  PMID: 23639954
Distyly; Exochaenium; floral evolution; Gentianaceae; herkogamy; heterostyly; phylogeny
2.  Ecological context and metapopulation dynamics affect sex-ratio variation among dioecious plant populations 
Annals of Botany  2013;111(5):917-923.
Background and Aims
Populations of dioecious flowering plants commonly exhibit heterogeneity in sex ratios and deviations from the equilibrium expectation of equal numbers of females and males. Yet the role of ecological and demographic factors in contributing towards biased sex ratios is currently not well understood.
Methods
Species-level studies from the literature were analysed to investigate ecological correlates of among-population sex-ratio variation and metapopulation models and empirical data were used to explore the influence of demography and non-equilibrium conditions on flowering sex ratios.
Key Results
The survey revealed significant among-population heterogeneity in sex ratios and this was related to the degree of sampling effort. For some species, sex-ratio bias was associated with the proportion of non-reproductive individuals, with greater male bias in populations with a lower proportion of individuals that were flowering. Male-biased ratios were also found at higher altitudes and latitudes, and in more xeric sites. Simulations and empirical data indicated that clonal species exhibited greater heterogeneity in sex ratios than non-clonal species as a result of their slower approach to equilibrium. The simulations also indicated the importance of interactions between reproductive mode and founder effects, with greater departures from equilibrium in clonal populations with fewer founding individuals.
Conclusions
The results indicate that sex-based differences in costs of reproduction and non-equilibrium conditions can each play important roles in affecting flowering sex ratios in populations of dioecious plants.
doi:10.1093/aob/mct040
PMCID: PMC3631328  PMID: 23444124
Biased sex ratios; costs of reproduction; dioecy; stress gradients; non-equilibrium conditions; metapopulations
3.  Rain pollination provides reproductive assurance in a deceptive orchid 
Annals of Botany  2012;110(5):953-958.
Background and Aims
Abiotic pollination by wind or water is well established in flowering plants. In some species pollination by rain splashes, a condition known as ombrophily, has been proposed as a floral strategy. However, evidence for this type of abiotic pollination has remained controversial and many reported cases have subsequently been shown to be false. This study investigates ombrophily in the deceptive orchid Acampe rigida to determine the mechanism by which this species is able to maintain high fecundity, despite flowering during the rainy season in south-west China when pollinators are scarce.
Methods
The floral mechanisms promoting rain pollination in A. rigida were observed and described in detail. Controlled pollination experiments and observations of floral visitors were conducted. A field experiment using rain shelters at 14 sites in Guangxi, south-west China, evaluated the contribution of rain pollination to fruit-set.
Key Results
During rainfall, raindrops physically flicked away the anther cap exposing the pollinarium. Raindrops then caused pollinia to be ejected upwards with the strap-like stipe pulling them back and causing them to fall into the stigmatic cavity, resulting in self-pollination. Neither flower nor pollen function were damaged by water. Although A. rigida is self-compatible, it is incapable of autonomous self-pollination without the assistance of rain splashes. The results of the rain-sheltering experiment indicated that rain pollination contributed substantially to increasing fruit-set, although there was variation among sites in the intensity of this effect.
Conclusions
A. rigida flowers during the rainy season, when pollinators are scarce, and ombrophily functions to provide reproductive assurance without compromising opportunities for outcrossing.
doi:10.1093/aob/mcs165
PMCID: PMC3448421  PMID: 22851311
Abiotic pollination; Acampe rigida; floral adaptation; ombrophily; rain-mediated self-pollination; deceptive orchid
4.  The natural history of pollination and mating in bird-pollinated Babiana (Iridaceae) 
Annals of Botany  2011;109(3):667-679.
Background and Aims
Floral variation, pollination biology and mating patterns were investigated in sunbird-pollinated Babiana (Iridaceae) species endemic to the Western Cape of South Africa. The group includes several taxa with specialized bird perches and it has been proposed that these function to promote cross-pollination.
Methods
Pollinator observations were conducted in 12 populations of five taxa (B. ringens subspp. ringens, australis, B. hirsuta, B. avicularis, B. carminea) and geographic variation in morphological traits investigated in the widespread B. ringens. Experimental pollinations were used to determine the compatibility status, facility for autonomous self-pollination and intensity of pollen limitation in six populations of four taxa. Allozyme markers were employed to investigate mating patterns in four populations of three species.
Key Results
Sunbirds were the primary pollinators of the five Babiana taxa investigated. Correlated geographical variation in perch size, flower size and stigma–anther separation was evident among B. ringens populations. Experimental pollinations demonstrated that B. ringens and B. avicularis were self-compatible with variation in levels of autonomous self-pollination and weak or no pollen limitation of seed set. In contrast, B. hirsuta was self-incompatible and chronically pollen limited. Estimates of outcrossing rate indicated mixed mating with substantial self-fertilization in all species investigated.
Conclusions
Despite the possession of specialized bird perches in B. ringens and B. avicularis, these structures do not prevent considerable selfing from occurring, probably as a result of autonomous self-pollination. In eastern populations of B. ringens, smaller flowers and reduced herkogamy appear to be associated with a shift to predominant selfing. Relaxed selection on perch function due to increased selfing may explain the increased incidence of apical flowers in some populations.
doi:10.1093/aob/mcr172
PMCID: PMC3278289  PMID: 21831856
Babiana; bird perch; sunbird pollination; floral variation; mating; pollen limitation; relaxed selection
5.  Floral dimorphism in plant populations with combined versus separate sexes 
Annals of Botany  2011;108(4):765-776.
Background and Aims
Dimorphism among floral traits can evolve through variation in selection intensity between female and male performance, especially when sex functions are separated between flowers on a plant (monoecy), or between individuals (dioecy). In animal-pollinated species, male floral traits are predicted to be larger because competition for pollinators should favour larger displays. Floral dimorphism may be greater in dioecious than monoecious populations because of trade-offs between female and male function and opportunities for selfing in hermaphrodites.
Methods
These predictions were tested by surveying flower size, total flowers per inflorescence and daily display size in the insect-pollinated Sagittaria latifolia (Alismataceae). This species is useful for comparative analysis because populations are mostly either monoecious or dioecious. We examined floral dimorphism in 13 monoecious and 16 dioecious populations in eastern North America.
Key Results
Male flowers were significantly larger than female flowers in monoecious and dioecious populations, but there was no evidence for greater flower size dimorphism in dioecious populations despite their larger flower sizes overall. Although inflorescences in both dioecious and monoecious populations produced more male flowers, daily floral displays were significantly larger for female than male function due to more synchronous female flower opening. Daily floral display dimorphism was significantly greater in dioecious populations, due to greater female daily floral displays. There was a positive relationship between mean flower size and total flowers per inflorescence for both sexes in dioecious populations, but no relationship for either sex function in monoecious populations. Flower size dimorphism was positively correlated with the frequencies of females in dioecious populations.
Conclusions
The increased size and number of male flowers and protracted male floral displays in S. latifolia are probably shaped by sexual selection for more effective pollen dispersal.
doi:10.1093/aob/mcr025
PMCID: PMC3170149  PMID: 21385777
Sexual dimorphism; flower size; daily floral display; sexual selection; sex ratios; monoecy; dioecy; Sagittaria latifolia
6.  Cryptic dioecy in Mussaenda pubescens (Rubiaceae): a species with stigma-height dimorphism 
Annals of Botany  2010;106(4):521-531.
Background and Aims
Evolutionary transitions from heterostyly to dioecy have been proposed in several angiosperm families, particularly in Rubiaceae. These transitions involve the spread of male and female sterility mutations resulting in modifications to the gender of ancestral hermaphrodites. Despite sustained interest in the gender strategies of plants, the structural and developmental bases for transitions in sexual systems are poorly understood.
Methods
Here, floral morphology, patterns of fertility, pollen-tube growth and floral development are investigated in two populations of the scandent shrub Mussaenda pubescens (Rubiaceae), native to southern China, by means of experimental and open-pollinations, light microscopy, fluorescence microscopy and scanning electron microscopy combined with paraffin sectioning.
Key Results
Mussaenda pubescens has perfect (hermaphroditic) flowers and populations with two style-length morphs but only weak differentiation in anther position (stigma-height dimorphism). Experimental pollinations demonstrated that despite morphological hermaphroditism, the species is functionally dioecious. The long-styled (L) morph possesses sterile pollen and functions as a female, whereas the short-styled (S) morph is female sterile and functions as a male. Self- and intra-morph pollinations of the S-morph were consistent with those expected from dimorphic incompatibility. The two populations investigated were both S-morph (male) biased. Investigations of early stages of floral development indicated patterns typical of hermaphroditic flowers, with no significant differences in organ growth between the floral morphs. Meiosis of microspore mother cells was of the simultaneous type with tetrads isobilateral in shape. The tapetal cells in anther walls of the L-morph became vacuolized during meiosis I, ahead of the uninucleate microspore stage in the S-morph. In the L-morph, the microspore nucleus degenerated at the tetrad stage resulting in male sterility. Microsporogenesis and male gametophyte development was normal in the S-morph. Failure in the formation of megaspore mother cells and/or the development of megagametophytes resulted in female sterility in the S-morph, compared with normal megasporogenesis in the L-morph.
Conclusions
In M. pubescens, cryptic dioecy has evolved from stigma-height dimorphism as a result of morph-specific sterility mutations.
doi:10.1093/aob/mcq146
PMCID: PMC2944971  PMID: 20647224
Dioecy; distyly; female and male sterility; floral development; Mussaenda pubescens; stigma-height polymorphism; self-incompatibility
7.  Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants 
Annals of Botany  2009;103(9):1515-1527.
Background
The rich literature that characterizes the field of pollination biology has focused largely on animal-pollinated plants. At least 10 % of angiosperms are wind pollinated, and this mode of pollination has evolved on multiple occasions among unrelated lineages, and hence this discrepancy in research interest is surprising. Here, the evolution and functional ecology of pollination and mating in wind-pollinated plants are discussed, a theoretical framework for modelling the selection of wind pollination is outlined, and pollen capture and the occurrence of pollen limitation in diverse wind-pollinated herbs are investigated experimentally.
Scope and Conclusions
Wind pollination may commonly evolve to provide reproductive assurance when pollinators are scarce. Evidence is presented that pollen limitation in wind-pollinated plants may not be as common as it is in animal-pollinated species. The studies of pollen capture in wind-pollinated herbs demonstrate that pollen transfer efficiency is not substantially lower than in animal-pollinated plants as is often assumed. These findings challenge the explanation that the evolution of few ovules in wind-pollinated flowers is associated with low pollen loads. Floral and inflorescence architecture is crucial to pollination and mating because of the aerodynamics of wind pollination. Evidence is provided for the importance of plant height, floral position, and stamen and stigma characteristics in promoting effective pollen dispersal and capture. Finally, it is proposed that geitonogamous selfing may alleviate pollen limitation in many wind-pollinated plants with unisexual flowers.
doi:10.1093/aob/mcp035
PMCID: PMC2701749  PMID: 19218583
Wind pollination; reproductive assurance; pollen limitation; geitonogamy; sex allocation; inflorescence architecture; mating systems
8.  Modification of flower architecture during early stages in the evolution of self-fertilization 
Annals of Botany  2009;103(6):951-962.
Background and Aims
The evolution of selfing from outcrossing is characterized by a series of morphological changes to flowers culminating in the selfing syndrome. However, which morphological traits initiate increased self-pollination and which are accumulated after self-fertilization establishes is poorly understood. Because the expression of floral traits may depend on the conditions experienced by an individual during flower development, investigation of changes in mating system should also account for environmental and developmental factors. Here, early stages in the evolution of self-pollination are investigated by comparing floral traits among Brazilian populations of Eichhornia paniculata (Pontederiaceae), an annual aquatic that displays variation in selfing rates associated with the breakdown of tristyly to semi-homostyly.
Methods
Thirty-one Brazilian populations under uniform glasshouse conditions were compared to investigate genetic and environmental influences on flower size and stigma–anther separation (herkogamy), two traits that commonly vary in association with transitions to selfing. Within-plant variation in herkogamy was also examined and plants grown under contrasting environmental conditions were compared to examine to what extent this trait exhibits phenotypic plasticity.
Key Results
In E. paniculata a reduction in herkogamy is the principal modification initiating the evolution of selfing. Significantly, reduced herkogamy was restricted to the mid-styled morph and occurred independently of flower size. Significant genetic variation for herkogamy was detected among populations and families, including genotypes exhibiting developmental instability of stamen position with bimodal distributions of herkogamy values. Cloned genets exposed to contrasting growth conditions demonstrated environmental control of herkogamy and genotypic differences in plasticity of this trait.
Conclusions
The ability to modify herkogamy independently of other floral traits, genetic variation in the environmental sensitivity of herkogamy, and the production of modified and unmodified flowers within some individuals, reveal the potential for dynamic control of the mating system in a species that commonly confronts heterogeneous aquatic environments.
doi:10.1093/aob/mcp015
PMCID: PMC2707899  PMID: 19202135
Eichhornia paniculata; expressivity; flower morphology; herkogamy; phenotypic plasticity; pleiotropy; population variation; self-fertilization; stigma–anther separation; outcrossing; tristyly
9.  High Outcrossing in the Annual Colonizing Species Ambrosia artemisiifolia (Asteraceae) 
Annals of Botany  2008;101(9):1303-1309.
Background and Aims
Variation in mating patterns may be particularly evident in colonizing species because they commonly experience wide variation in plant density. Here, the role of density for the mating system of Ambrosia artemisiifolia (common ragweed), a wind-pollinated annual colonizing species previously reported as self-compatible, is explored.
Methods
The effect of population density on the proportion of self- and cross-fertilized seeds was examined using allozyme markers and experimental arrays conducted over two seasons in the field. Also the reproductive success of isolated plants located in diverse habitats was measured. The potential occurrence of a physiological mechanism preventing self-fertilization, i.e. self-incompatibility, following controlled self- and cross-pollinations in the glasshouse was examined.
Key Results
Outcrossing rates estimated using allozyme markers were uniformly high, regardless of the spacing between plants. However, when single plants were isolated from congeners they set few seeds. Observations of pollen-tube growth and seed set following controlled pollinations demonstrated that plants of A. artemisiifolia possess a strong self-incompatibility mechanism, contrary to earlier reports and assumptions.
Conclusions
The maintenance of high outcrossing rates in colonizing populations of A. artemisiifolia is likely to be facilitated by the prodigious production of wind-borne pollen, high seed production and extended seed dormancy.
doi:10.1093/aob/mcn039
PMCID: PMC2710250  PMID: 18387973
Self-incompatibility; outcrossing rate; density dependence; colonization; wind-pollination; Ambrosia artemisiifolia (ragweed); Asteraceae

Results 1-9 (9)