Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured

Flowering times of plants are important life-history components and it has previously been hypothesized that flowering phenologies may be currently subject to natural selection or be selectively neutral. In this study we reviewed the evidence for phenotypic selection acting on flowering phenology using ordinary and phylogenetic meta-analysis. Phenotypic selection exists when a phenotypic trait co-varies with fitness; therefore, we looked for studies reporting an association between two components of flowering phenology (flowering time or flowering synchrony) with fitness. Data sets comprising 87 and 18 plant species were then used to assess the incidence and strength of phenotypic selection on flowering time and flowering synchrony, respectively. The influence of dependence on pollinators, the duration of the reproductive event, latitude and plant longevity as moderators of selection were also explored. Our results suggest that selection favours early flowering plants, but the strength of selection is influenced by latitude, with selection being stronger in temperate environments. However, there is no consistent pattern of selection on flowering synchrony. Our study demonstrates that phenotypic selection on flowering time is consistent and relatively strong, in contrast to previous hypotheses of selective neutrality, and has implications for the evolution of temperate floras under global climate change.     

迁地保育植物花期物候对迁入地气候变化的响应

以中国科学院武汉植物园内栽培的长果秤锤树(Sinojackia dolichocarpa C. J. Qi)、山白树(Sinowilsonia henryi Hemsl.)、夏腊梅(Sinocalycanthus chinensis Cheng et S. Y. Chang)、紫茎(Stewartia sinensis Rehd. et Wils.)和绒毛皂荚(Gleditsia vestita Chun et How ex B. G. Li) 5种迁地保育植物为对象,通过2008-2016年观察记录的初花期物候及整个花期长度的数据,研究花期的年际变化规律及其与迁入地武汉气候因子的相关性。结果显示:(1)从初花期来看,长果秤锤树的初花期每年提前1.25 d,紫茎的初花期每年推迟1.35 d,绒毛皂荚的初花期每年推迟1.22 d。(2)从花期长度来看,山白树的花期每年增加1.72 d,夏蜡梅的花期每年减少1.62 d,紫茎的花期每年增加0.32 d。(3)从花期与气候因子的相关性来看,年降水量、年平均相对湿度、 10℃有效积温、花前 10℃的有效积温是影响这5种植物初花期、花期长度的主要气候因子;不同物种间影响花期的主要气候因子有所差异。     

Global warming and the disruption of plant-pollinator interactions

Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO₂. Depending on model assumptions, phenological shifts reduced the floral resources available to 17–50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.     

Phenotypic selection on flowering phenology and size in two dioecious plant species with different pollen vectors

Dioecious plants may be pollinated biotically by animals or abiotically via wind or water currents. It has been hypothesized that these two types of pollen vectors might impose contrasting selective pressures on plant flowering phenology. In the present study we describe the flowering phenology of two sympatric dioecious species with contrasting pollination modes: Mercurialis perennis (wind‐pollinated) and Tamus communis (insect‐pollinated). We estimated selection differentials and gradients for flowering time and flowering synchrony. As flowering time might depend on the accumulation of enough internal resources, we also estimated direct and indirect selection on plant size. Both species have male‐biased sexual ratios, and males are bigger and produce larger flower displays than females, but only in T. communis do males bloom earlier and for longer than females. Selection gradients suggest that selection tends to favor early‐flowering females of T. communis. There is no evidence of direct current selection on the flowering phenology of M. perennis. Intersexual differences in phenology fit with sex allocation and sexual selection theories. As we hypothesized, phenology of the animal‐pollinated species is under stronger selection than that of the wind‐pollinated species and we discuss the potential role of pollen vectors in shaping the flowering phenologies of the study species.     

Divergent selection on flowering phenology but not on floral morphology between two closely related orchids

Closely related species often differ in traits that influence reproductive success, suggesting that divergent selection on such traits contribute to the maintenance of species boundaries. Gymnadenia conopsea ss. and Gymnadenia densiflora are two closely related, perennial orchid species that differ in (a) floral traits important for pollination, including flowering phenology, floral display, and spur length, and (b) dominant pollinators. If plant–pollinator interactions contribute to the maintenance of trait differences between these two taxa, we expect current divergent selection on flowering phenology and floral morphology between the two species. We quantified phenotypic selection via female fitness in one year on flowering start, three floral display traits (plant height, number of flowers, and corolla size) and spur length, in six populations of G. conopsea s.s. and in four populations of G. densiflora. There was indication of divergent selection on flowering start in the expected direction, with selection for earlier flowering in two populations of the early‐flowering G. conopsea s.s. and for later flowering in one population of the late‐flowering G. densiflora. No divergent selection on floral morphology was detected, and there was no significant stabilizing selection on any trait in the two species. The results suggest ongoing adaptive differentiation of flowering phenology, strengthening this premating reproductive barrier between the two species. Synthesis: This study is among the first to test whether divergent selection on floral traits contribute to the maintenance of species differences between closely related plants. Phenological isolation confers a substantial potential for reproductive isolation, and divergent selection on flowering time can thus greatly influence reproductive isolation and adaptive differentiation.     

Diversification of floral orientation in Lonicera is associated with pollinator shift and flowering phenology

Floral orientation has been suggested to be a functional floral trait that can enhance reproductive fitness through adaptation to both biotic factors (e.g., pollination) and abiotic factors (e.g., temperature). However, whether those factors drive the diversification of floral orientation needs to be explored through multiple related species. Phylogenetic relationships in Lonicera were identified by incorporating the species’ floral orientation (upward vs. downward) and pollinator types. Furthermore, transitions in floral orientation were evaluated together with pollinator shift, and seven Lonicera species were used to detect the influence of floral orientation on pollination and reproductive success. The relationship between temperature and the angle of floral orientation was investigated. Floral orientation in Lonicera showed that most of the closely related species within the same node displayed a similar pattern of floral orientation, and pollinator shift can lead to transitions between upward and downward orientation. Additionally, the angle of floral orientation increased with flowering phenology from spring to summer, and changing floral orientation significantly decreased pollination and seed production. Moreover, the average daily temperature during flowering phenology was significantly correlated with the angle of floral orientation. Our results indicate that pollinator shift could be an important event, leading to the diversification of floral orientation. Results of field investigations inferred that floral orientation should be a functional floral trait adapted to flowering phenology. Downward-facing flowers might help decrease heat loss to adapt to cold conditions. This study disentangled the influences of historical events and local adaptation on the evolution of floral orientation.     

Effects of experimentally imposed climate scenarios on flowering phenology and flower production of subarctic bog species

Climate scenarios for high‐latitude areas predict not only increased summer temperatures, but also larger variation in snowfall and winter temperatures. By using open‐top chambers, we experimentally manipulated both summer temperatures and winter and spring snow accumulations and temperatures independently in a blanket bog in subarctic Sweden, yielding six climate scenarios. We studied the effects of these scenarios on flowering phenology and flower production of Andromeda polifolia (woody evergreen) and Rubus chamaemorus (perennial herb) during 2 years. The second year of our study (2002) was characterized by unusually high spring and early summer temperatures. Our winter manipulations led to consistent increases in winter snow cover. As a result, average and minimum air and soil temperatures in the high snow cover treatments were higher than in the winter ambient treatments, whereas temperature fluctuations were smaller. Spring warming resulted in higher average, minimum, and maximum soil temperatures. Summer warming led to higher air and soil temperatures in mid‐summer (June–July), but not in late summer (August–September). The unusually high temperatures in 2002 advanced the median flowering date by 2 weeks for both species in all treatments. Superimposed on this effect, we found that for both Andromeda and Rubus, all our climate treatments (except summer warming for Rubus) advanced flowering by 1–4 days. The total flower production of both species showed a more or less similar response: flower production in the warm year 2002 exceeded that in 2001 by far. However, in both species flower production was only stimulated by the spring‐warming treatments. Our results show that the reproductive ecology of both species is very responsive to climate change but this response is very dependent on specific climate events, especially those that occur in winter and spring. This suggests that high‐latitude climate change experiments should focus more on winter and spring events than has been the case so far.     

Evolution of mutualism in plant-pollinator interactions on islands

The evolution and ecology of interactions between plants and pollinators are discussed based on the studies on the Izu Islands and mainland Honshu, Japan. The species assemblage is depauperate, and long-tongued pollinators are absent or rare on the islands. Bumblebees, one of the most important pollinators in Japan, are generally absent. Plants depending strongly on bumblebee pollination are absent on Izu Islands, but those depending on varied pollinators including bumblebees display smaller flower sizes and accommodate smaller pollinators than their mainland counterparts. Breeding systems of these species also shift to partial inbreeding, possibly an evolutionary result of the decrease in pollinator availability. Changes in flowering phenology between mainland and island populations also occur. Plants in the islands tend to reproduce vegetatively less frequently and produce greater numbers of smaller seeds than those in the mainland. The possibility of evolution on the side of island pollinator species is also discussed, although there are few data on this topic.     

The effects of phenological mismatches on demography

Climate change is altering the phenology of species across the world, but what are the consequences of these phenological changes for the demography and population dynamics of species? Time-sensitive relationships, such as migration, breeding and predation, may be disrupted or altered, which may in turn alter the rates of reproduction and survival, leading some populations to decline and others to increase in abundance. However, finding evidence for disrupted relationships, or lack thereof, and their demographic effects, is difficult because the necessary detailed observational data are rare. Moreover, we do not know how sensitive species will generally be to phenological mismatches when they occur. Existing long-term studies provide preliminary data for analysing the phenology and demography of species in several locations. In many instances, though, observational protocols may need to be optimized to characterize timing-based multi-trophic interactions. As a basis for future research, we outline some of the key questions and approaches to improving our understanding of the relationships among phenology, demography and climate in a multi-trophic context. There are many challenges associated with this line of research, not the least of which is the need for detailed, long-term data on many organisms in a single system. However, we identify key questions that can be addressed with data that already exist and propose approaches that could guide future research.     

开花时间与伴生种对鹤首马先蒿传粉和生殖成功的影响

开花物候是物种间相互作用的重要生活史特征和适合度因子,在全球气候变化的背景下而备受关注.为探讨开花时间如何存种内和种间水平上影响植物的传粉和生殖成功,我们连续3年(2003-2005)对不同花期和伴生种存在情况下的鹤首马先蒿(Pedicularis gruina)的传粉者访花忠实度、受粉率、坐果率、单果种子产量和果实被啃食频率进行了比较研究.结果表明鹤首马先蒿的坐果率主要受其传粉环境的影响:在没有伴生种时,不同时期鹤首马先蒿的坐果率没有显著差异,34-38％的花可以坐果;在有伴生种存在时既可以显著提高其坐果率,也可显著降低其坐果率,这取决于传粉者类型以及伴生种密穗马先蒿(P.densispica)花期的差异.密穗马先蒿具有花蜜和花粉双重报酬,在群落中可以作为主体物种吸引传粉者并间接促进与其伴生的鹤首马先蒿的传粉和生殖成功.同样无蜜的管花马先蒿(P.siphonantha)和鹤首马先蒿伴生,则是通过提高群落水平对传粉者的吸引力进而直接促进鹤首马先蒿的传粉和生殖成功.此外,研究结果也表明开花时间对坐果率没有显著影响,但是显著影响单果种子产量和果实被啃食的频率.在相同的传粉条件下早花期植株单果种子产量显著高于晚花期的种子产量,同时早花期的果实被啃食的频率显著增加.     

Apple (Malus pumila var. domestica) phenology is advancing due to rising air temperature in northern Japan

Recent studies show advancing onset of plant growing season in many regions for the last several decades. With the well‐established dependence of plant phenology on temperature, these trends are interpreted as an indication of global warming. For several decades, however, other determinants of plant phenology, e.g. varieties and trends in managed systems, may have changed and confounded the phenological trends. In this study, we tested if long‐term changes in phenology of apple (Malus pumila var. domestica) are attributable to long‐term changes in temperature by comparing the phenological response to long‐term trend in air temperature, which is of our interest, with that to year‐to‐year fluctuation in air temperature, which should represent the real effect of temperature on phenology. We collected records of air temperature and phenological events (budding and flowering) in apple from 1977 to 2004 at six locations in Japan. Linear trends in flowering showed advancing rate in the range from 0.21 to 0.35 day yr^?1, statistically significant at three locations (P<0.05). We also found a warming trend in mean air temperature throughout March and April, with which flowering was closely correlated, in the range from 0.047 to 0.077 °C yr^?1, statistically significant at five locations (P<0.05). We separated the temperature time‐series into two components: a long‐term trend and a year‐to‐year fluctuation, by fitting smoothing spline to the trend and taking the residuals as the anomaly. We then fit a multiple regression model of phenological response to air temperature with separate coefficients for long‐term trend and anomaly. Flowering date responded to the long‐term trend at ?3.8 day °C^?1 and to the anomaly at ?4.6 day °C^?1. The temperature coefficients were not statistically different from each other or among locations, suggesting that the advance of apple phenology has predominantly been caused by the temperature increase across the locations studied. The same result was also observed with budding.     

Flowering phenology of a palm community in a central Amazon forest

The flowering phenology of 27 taxa of palms in a lowland moist forest in the central Amazon was recorded over a 40 month period. Phenological data were transformed into measures, of synchrony, regularity, and duration. Flowering was observed at all times of year and there was no correlation with rainfall either for the current month or for any monthly lag interval. The 27 taxa were divided into three pollination groups—weevil, bee/fly, or beetle—based on their behavior at anthesis. Phenology was significantly correlated with pollination groups. Weevilpollinated palms had higher synchrony and shorter duration of flowering than other groups. Bee/fly-pollinated palms had lower synchrony and longer duration of flowering. The beetle-pollinated palms were intermediate between the two other groups. Seasonal regularity of flowering was similar in all three groups. We suggest that, at least inBactris, taxa exhibit staggered flowering.     

Direct and indirect effects of episodic frost on plant growth and reproduction in subalpine wildflowers

Frost is an important episodic event that damages plant tissues through the formation of ice crystals at or below freezing temperatures. In montane regions, where climate change is expected to cause earlier snow melt but may not change the last frost‐free day of the year, plants that bud earlier might be directly impacted by frost through damage to flower buds and reproductive structures. However, the indirect effects of frost mediated through changes in plant–pollinator interactions have rarely been explored. We examined the direct and pollinator‐mediated indirect effects of frost on three wildflower species in southwestern Colorado, USA, Delphinium barbeyi (Ranunculaceae), Erigeron speciosus (Asteraceae), and Polemonium foliosissimum (Polemoniaceae), by simulating moderate (?1 to ?5°C) frost events in early spring in plants in situ. Subsequently, we measured plant growth, and upon flowering measured flower morphology and phenology. Throughout the flowering season, we monitored pollinator visitation and collected seeds to measure plant reproduction. We found that frost had species‐specific direct and indirect effects. Frost had direct effects on two of the three species. Frost significantly reduced flower size, total flowers produced, and seed production of Erigeron. Furthermore, frost reduced aboveground plant survival and seed production for Polemonium. However, we found no direct effects of frost on Delphinium. When we considered the indirect impacts of frost mediated through changes in pollinator visitation, one species, Erigeron, incurred indirect, negative effects of frost on plant reproduction through changes in floral traits and pollinator visitation, along with direct effects. Overall, we found that flowering plants exhibited species‐specific direct and pollinator‐mediated indirect responses to frost, thus suggesting that frost may play an important role in affecting plant communities under climate change.     

Impact of plant flowering phenology on the cost/benefit balance in a nursery pollination mutualism,with honest males and cheating females

This study documents the flowering phenology and its potential consequences on a nursery pollination mutualism between a dioecious plant, in which honest male plants, but not cheating females, allow the specific pollinator to reproduce within inflorescences. Very few pollinators were found to emerge during plant anthesis, leading to a low (if any) potential benefit through pollen dispersal. This opens the question why male plants do not also cheat their pollinators. Female plants flowered late in the season, when many males had just achieved their own anthesis, which increased the efficiency of pollen transfer. Finally, some late‐flowering males reached their anthesis simultaneously with females, which open the possibility for pollinator to choose between honest males and cheating females. Nevertheless, female plants were found to produce fruits, even though fruit production was limited by pollen (and pollinator) supply, meaning that cheating was not entirely retaliated by the mutualistic partner.     

Selection on flowering time and floral display in an alpine and a lowland population of Arabidopsis lyrata

To determine whether population differentiation in flowering time is consistent with differences in current selection, we quantified phenotypic selection acting through female reproductive success on flowering phenology and floral display in two Scandinavian populations of the outcrossing, perennial herb Arabidopsis lyrata in two years. One population was located in an alpine environment strongly affected by grazing, whereas the other was close to sea level and only moderately affected by herbivory. Multiple regression models indicated directional selection for early end of flowering in one year in the lowland population, and directional selection for early start of flowering in one year in the alpine population. As expected, there was selection for more inflorescences in the lowland population. However, in the alpine population, plants with many inflorescences were selectively grazed and the number of inflorescences produced was negatively related to female fitness in one year and not significantly related to female fitness in the second year. The results are consistent with the hypothesis that genetic differentiation in flowering phenology between the study populations is adaptive, and indicate that interactions with selective grazers may strongly influence selection on floral display in A. lyrata.     

全球气候变暖影响植物-传粉者网络的研究进展

植物与传粉者间相互作用,构成了复杂的传粉网络。目前,以气候变化为主要特征的全球变暖对植物-传粉者网络的影响备受关注,概述了近年来这方面研究的几个主要热点问题及其进展,和相关研究方法。并在此基础上,提出了气温持续上升背景下,植物-传粉者网络未来的研究趋势。当前研究的主要热点问题有:(1)气候变暖使植物、传粉者的物候发生变化,并通过影响植物的开花时间和传粉者活动时间,导致两者在物候时间上的不同步。(2)气候变暖导致植物、传粉者的群落结构变化,促使其地理分布向更高纬度和更高海拔扩散,这可能潜在的导致两者空间分布的不匹配。(3)植物和传粉者通过增加或减少其丰富度来响应气候变暖,可能导致传粉网络结构特征发生变化。(4)面对气候变暖导致植物和传粉者间物候和地理分布错配所引发的互作改变、甚至解体,传粉网络可通过自身网络结构及快速进化来缓冲和适应。在今后研究中,以下几个问题值得探讨:1)气候变暖对植物-传粉者网络影响的大时空尺度变异模式。2)多因素协同作用对植物-传粉者网络的影响特征。3)全球气候变暖对植物、传粉者物候匹配性影响的机理。     

Effects of climate warming on host–parasitoid interactions

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