Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing ‘division of labour'' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant–pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male–male competition for siring success.     

软枣猕猴桃控制授粉对果实和种子的影响

为了研究软枣猕猴桃授粉规律,以11年生软枣猕猴桃紫果3号为试验材料,设置剪留花柱数量为0、2、5、8、11、14、17和23(全留对照组)共8个处理。人工授粉,收获后调查测定其单果重、坐果率、果型指数、果实可溶性固形物含量和果实内含种子数量。结果表明:随着授粉柱头数的增加,单果重等主要指标相应增加;当授粉柱头数增至为8时,其果型指数和果实可溶性固形物含量与对照全留柱头23相比差异不明显;当授粉柱头数增至为11时,其单果重、坐果率和果实内含种子数量与对照全留柱头23相比差异不明显。据此软枣猕猴桃充分授粉的数量级指标为11,当授粉柱头数小于11时,产量降低、品质下降;当授粉柱头大于11时,浪费花粉。生产上可利用猕猴桃精准充分授粉技术,节约使用花粉或减少果园雄株数量,以提高生产效率。     

Flower biology of the cactus Coryphantha elephantidens in the tropical dry forest of Central Mexico

Floral traits and sexual systems in angiosperms are strategies that enhance outcrossing within hermaphrodite flowers and among individuals in a population. Sexual systems with unisexual flowers have also evolved among angiosperms, resulting in sex specialization. Furthermore, the interaction of floral traits and floral visitors determines successful plant reproduction. Globose cacti are bee pollinated, and variation in the diversity of their pollinator assemblages is strongly associated with floral phenotype. Our objective was to describe the floral biology of the cactus Coryphantha elephantidens and to determine its relationship with pollinators. Floral traits were studied by direct observations in live and fixed flowers. The breeding system was determined using two estimators based on floral morphology: pollen grains to ovules per flower (P/O) ratio and outcrossing index. Pollination treatments were conducted to determine the mating system. Floral visitors were recorded using direct observation. Flowers of C. elephantidens are variable in color, protandric, herkogamous and nectarless. Estimators of the breeding system indicated xenogamy, which is consistent with the obligate outcrossing revealed by the pollination experiment. Thirty-seven percent of the plants have female flowers that do not produce pollen, making this population functionally gynodioecious. Both fruit and seed set were high compared to other globose cacti. Pollinators included eight species of native bees, a more diverse pollinator assemblage than other globose cacti. Given the high pressure on pollen due to functional gynodioecy, nectarless flowers, an outcrossing mating system, and the necessity of pollinators to set seeds, we concluded that native bees are highly efficient pollinators that play a crucial role in the sexual reproduction of C. elephantidens.     

Environmentally induced phenotypic plasticity and DNA methylation changes in a wild potato growing in two contrasting Andean experimental gardens

DNA methylation can be environmentally modulated and plays a role in phenotypic plasticity. To understand the role of environmentally induced epigenetic variation and its dynamics in natural populations and ecosystems, it is relevant to place studies in a real-world context. Our experimental model is the wild potato Solanum kurtzianum, a close relative of the cultivated potato S. tuberosum. It was evaluated in its natural habitat, an arid Andean region in Argentina characterised by spatial and temporal environmental fluctuations. The dynamics of phenotypic and epigenetic variability (with Methyl Sensitive Amplified Polymorphism markers, MSAP) were assayed in three genotypes across three growing seasons. These genotypes were cultivated permanently and also reciprocally transplanted between experimental gardens (EG) differing in ca. 1000 m of altitude. In two seasons, the genotypes presented differential methylation patterns associated to the EG. In the reciprocal transplants, a rapid epigenomic remodelling occurred according to the growing season. Phenotypic plasticity, both spatial (between EGs within season) and temporal (between seasons), was detected. The epigenetic and phenotypic variability was positively correlated. The lack of an evident mitotic epigenetic memory would be a common response to short-term environmental fluctuations. Thus, the environmentally induced phenotypic and epigenetic variation could contribute to populations persistence through time. These results have implications for understanding the great ecological diversity of wild potatoes.     

传粉昆虫下降背景下的授粉生态弹性: 内涵、机制和展望

全球传粉昆虫多样性正在下降, 如何保障农林生态系统传粉功能是当前研究的热点。理论上说, 传粉功能不仅与生态系统的传粉昆虫多样性相关, 还与生态系统的调节能力有关。近年来, 学者们逐渐认识到授粉生态弹性对传粉功能的影响。本文在回顾已有研究的基础之上, 总结传粉昆虫授粉生态弹性的内涵, 厘清授粉生态弹性与工程弹性、稳定性和抗性的异同。目前, 学者对授粉生态弹性形成机制开展广泛探讨, 提出功能冗余假说、密度补偿假说、响应多样性假说、连接周转假说和跨尺度弹性假说, 但这5个假说间的关系仍不清楚, 存在一词多义、词意混淆等现象。我们依次阐述功能冗余假说、密度补偿假说、响应多样性假说、连接周转假说和跨尺度弹性假说, 介绍不同假说中授粉生态弹性形成过程、研究热点和发展动态。通过解析授粉生态弹性的形成机制可知, 5个假说在内涵上存在紧密联系, 它们从不同空间尺度和研究对象下解释传粉昆虫授粉生态弹性的形成机制。未来授粉生态弹性研究将整合传粉昆虫群落动态和传粉功能动态的量化方法, 通过实验验证5个假说的合理性, 并揭示不同假说间的联系, 由此阐明授粉生态弹性的发生条件、形成阈值和动态规律。随着研究的深入, 授粉生态弹性理论有望用于指导农林生态系统传粉功能的经营管理。     

The pollination of Habenaria rhodocheila (Orchidaceae) in South China: When butterflies take sides

Habenaria is one of the largest terrestrial genera in the family Orchidaceae. Most field studies on Habenaria species with greenish–white and nocturnal scented flowers are pollinated by nocturnal hawkmoths and settling moths. However, H. rhodocheila presents reddish flowers lacking a detectable scent and fails to fit the moth pollination syndrome. We investigated the pollinators, breeding system, and functional traits of H. rhodocheila in South China and found that two diurnal swallowtail butterflies Papilio helenus and Papilio nephelus (Papilionidae) were the effective pollinators. When butterflies foraged for nectar in the spur, the pollinia became attached between the palpi. A triangular projected median rostellar lobe was found at the entrance (sinus) of the spur of H. rhodocheila. This lobe divided the spur opening into two entrances forcing butterflies to enter their proboscides through the left or right side. When the projection of median rostellar lobe was removed, the site of pollinium attachment changed to the eyes of the butterflies, leading to a higher rate of pollinium removal but lower rate of pollinium deposition. Our quartz glass cylinder choice experiment suggested that visual rather than olfactory cues provided the major stimuli for butterflies to locate these flowers. Hand pollination experiments suggested this species was self‐compatible but pollinator‐dependent. However, the proportion of seeds with large embryos produced in self‐pollinated fruits was significantly lower than in cross‐pollinated fruits, indicating a significant inbreeding depression. Unlike many other orchid species, fruit set was higher than rates of pollinium removal, indicating a high level of pollination efficiency in a species with friable pollinia. Shifts from moth to butterfly pollination in the genus Habenaria parallel other orchid lineages providing insights into the potential for pollinator‐mediated floral trait selection.     

Nectar sugar composition of European Caryophylloideae (Caryophyllaceae) in relation to flower length,pollination biology and phylogeny

Floral nectar composition has been explained as an adaptation to factors that are either directly or indirectly related to pollinator attraction. However, it is often unclear whether the sugar composition is a direct adaptation to pollinator preferences. Firstly, the lower osmolality of sucrose solutions means that they evaporate more rapidly than hexose solutions, which might be one reason why sucrose‐rich nectar is typically found in flowers with long tubes (adapted to long‐tongued pollinators), where it is better protected from evaporation than in open or short‐tubed flowers. Secondly, it can be assumed that temperature‐dependent evaporation is generally lower during the night than during the day so that selection pressure to secrete nectar with high osmolality (i.e. hexose‐rich solutions) is relaxed for night‐active flowers pollinated at night. Thirdly, the breeding system may affect selection pressure on nectar traits; that is, for pollinator‐independent, self‐pollinated plants, a lower selective pressure on nectar traits can be assumed, leading to a higher variability of nectar sugar composition independent of pollinator preferences, nectar accessibility and nectar protection. To analyse the relations between flower tube length, day vs. night pollination and self‐pollination, the nectar sugar composition was investigated in 78 European Caryophylloideae (Caryophyllaceae) with different pollination modes (diurnal, nocturnal, self‐pollination) using high‐performance liquid chromatography (HPLC). All Caryophylleae species (Dianthus and relatives) were found to have nectar with more than 50% sucrose, whereas the sugar composition of Sileneae species (Silene and relatives) ranged from 0% to 98.2%. In the genus Silene, a clear dichotomous distribution of sucrose‐ and hexose‐dominant nectars is evident. We found a positive correlation between the flower tube length and sucrose content in Caryophylloideae, particularly in day‐flowering species, using both conventional analyses and phylogenetically independent contrasts.     

Pollen limitation and fruit abortion in a declining rare tree,the Eurasian yew (Taxus baccata L.): A reproductive cost of ecological marginality

Populations of rare tree species such as the dioecious and anemophilous yew (Taxus baccata) are especially prone to extinction if they occupy marginal habitats. This is the case of yew populations growing in Mediterranean mountains under dry climate and a severe anthropogenic disturbance regime, which show insufficient regeneration. We examined two of the likely mechanisms driving this population decline. The study was conducted in a central Spanish yew population in 2005 and 2006. On one hand, we tested for the effect of the amount of pollen received by female flowers by means of a pollen addition experiment. On the other hand, we tested for the effect of initial fruit set on abortion and mature fruit production. Finally, we evaluated the effect of the spatial arrangement of male and female yew trees on realized fecundity. The success of fertilization and fruiting in the experimental population was pollen-limited. Female trees aborted ca. 70% of the fruit set in both years and treatments. Fruit set was significantly influenced by the females' neighbourhood, with fecundity decreasing exponentially with distance to the nearest male in both years. Overall, our results indicate that factors associated with ecological marginality have a strong influence on yew performance.     

Effect of habitat disturbance on pollination biology of the columnar cactus Stenocereus quevedonis at landscape‐level in central Mexico

Stenocereus quevedonis (‘pitire’) is a columnar cactus endemic to central Mexico, grown for its edible fruit. Phenology, pollination biology and behaviour of flower visitors of this species were compared in six conserved and disturbed sites, hypothesising that: (i) pitire pollination is self‐incompatible, requiring animal vectors; (ii) higher incidence of radiation on plants in cleared forest may lead to a higher number of flowers per pitire plant and longer blooming season, and disturbing and differential spatial availability of flower resources may determine differential attraction of pollinators to conserved and disturbed areas; (iii) if pitire pollination system is specialised, reproductive success would decrease with pollinator scarcity, or other species may substitute for main pollinators. In all sites, pitire reproduction started in January, flowering peak occurring in April, anthesis duration was 15 h and predominantly nocturnal (9 h), pollen was released at 23:00 h, nectar was produced throughout anthesis, and breeding system was self‐incompatible. Flower production per plant was similar in disturbed and conserved sites, but flower availability was higher (because of higher tree density) and longer in disturbed sites. Pollination is nocturnal, the most frequent legitimate pollinator being the bat Leptonycteris yerbabuenae; diurnal pollination is rare but possible, carried out by bee species. Fruit and seed set in control and nocturnal pollination treatments at disturbed sites were higher than in conserved sites. Frequency of L. yerbabuenae visits was similar among site types, but more visits of complementary nocturnal and diurnal pollinators were recorded in disturbed sites, which could explain differences in reproductive success.     

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae)

Inga species present brush‐type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self‐incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose‐dominant (just after flower opening, when hummingbirds were the main visitors) to hexose‐rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.