Soil microbes alter plant fitness under competition and drought

Plants exist across varying biotic and abiotic environments, including variation in the composition of soil microbial communities. The ecological effects of soil microbes on plant communities are well known, whereas less is known about their importance for plant evolutionary processes. In particular, the net effects of soil microbes on plant fitness may vary across environmental contexts and among plant genotypes, setting the stage for microbially mediated plant evolution. Here, we assess the effects of soil microbes on plant fitness and natural selection on flowering time in different environments. We performed two experiments in which we grew Arabidopsis thaliana genotypes replicated in either live or sterilized soil microbial treatments, and across varying levels of either competition (isolation, intraspecific competition or interspecific competition) or watering (well‐watered or drought). We found large effects of competition and watering on plant fitness as well as the expression and natural selection of flowering time. Soil microbes increased average plant fitness under interspecific competition and drought and shaped the response of individual plant genotypes to drought. Finally, plant tolerance to either competition or drought was uncorrelated between soil microbial treatments suggesting that the plant traits favoured under environmental stress may depend on the presence of soil microbes. In summary, our experiments demonstrate that soil microbes can have large effects on plant fitness, which depend on both the environment and individual plant genotype. Future work in natural systems is needed for a complete understanding of the evolutionary importance of interactions between plants and soil microorganisms.     

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.     

Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus

Plant fitness is strongly affected by flowering phenology, and there are several ecological factors that are thought to shape the distribution of flowering times. One relatively underexamined factor is the timing and intensity of attack by herbivores that feed on flowers or developing seeds. This study tests the hypothesis that herbivores that feed on developing seeds of wild sunflower, Helianthus annuus (Asteraceae), impose selection on flowering phenology. First, the study population was found to contain genetic variation for mean date of flowering, so this trait could evolve if natural selection were operating. Next, the phenological pattern of abundance of five seed-feeding herbivores was documented. Damage by three herbivores, Haplorhynchites aeneus (Cucurlionidae), the head-clipping weevil, Homoeosoma electellum (Lepidoptera: Pyralidae), the sunflower moth, and Suleima helianthana (Lepidoptera: Tortricidae), the sunflower bud moth, was highest early in the flowering season, and declined as the season progressed. Damage by one herbivore, the seed fly Gymnocarena diffusa (Diptera: Tephrididae), was lowest early in the flowering season and increased as the season progressed. Finally, damage by two seed weevils, Smicronyx fulvus and S. sordidus (Curculionidae), whose damage was not distinguished, was constant through the flowering period. Third, damage by Haplorhynchites, Homoeosoma, and Suleima was found to be detrimental to plant fitness, suggesting that plants that flower when these herbivores are not abundant should have higher fitness. Finally, two phenotypic selection analyses were performed. The first included damage by Homoeosoma and Suleima, as well as flowering date, leaf area, and inflorescence diameter, as characters predicting plant fitness. In this analysis directional selection was found to act to decrease damage by the two herbivores, but did not act on flowering date. The second selection analysis was identical except that damage by the two herbivores was not included. In this analysis significant directional selection was found to favor later-flowering plants. Comparison of these two analyses suggests that all selection on flowering phenology is attributable to damage by Homoeosoma and Suleima: plants that flower later avoid damage by these two herbivores. While other influences on flowering phenology, such as pollination, mate availability, and seasonality, have been well documented, this study is one of few to demonstrate natural selection on flowering phenology that is a direct consequence of insect attack. Received: 17 November 1998 / Accepted: 18 July 1999     

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.     

Response to joint selection on germination and flowering phenology depends on the direction of selection

Flowering and germination time are components of phenology, a complex phenotype that incorporates a number of traits. In natural populations, selection is likely to occur on multiple components of phenology at once. However, we have little knowledge of how joint selection on several phenological traits influences evolutionary response. We conducted one generation of artificial selection for all combinations of early and late germination and flowering on replicated lines within two independent base populations in the herb Campanula americana. We then measured response to selection and realized heritability for each trait. Response to selection and heritability were greater for flowering time than germination time, indicating greater evolutionary potential of this trait. Selection for earlier phenology, both flowering and germination, did not depend on the direction of selection on the other trait, whereas response to selection to delay germination and flowering was greater when selection on the other trait was in the opposite direction (e.g., early germination and late flowering), indicating a negative genetic correlation between the traits. Therefore, the extent to which correlations shaped response to selection depended on the direction of selection. Furthermore, the genetic correlation between timing of germination and flowering varies across the trait distributions. The negative correlation between germination and flowering time found when selecting for delayed phenology follows theoretical predictions of constraint for traits that jointly determine life history schedule. In contrast, the lack of constraint found when selecting for an accelerated phenology suggests a reduction of the covariance due to strong selection favoring earlier flowering and a shorter life cycle. This genetic architecture, in turn, will facilitate further evolution of the early phenology often favored in warm climates.     

The causes of selection on flowering time through male fitness in a hermaphroditic annual plant

Flowering is a key life‐history event whose timing almost certainly affects both male and female fitness, but tests of selection on flowering time through male fitness are few. Such selection may arise from direct effects of flowering time, and indirect effects through covariance between flowering time and the environment experienced during reproduction. To isolate these intrinsically correlated associations, we staggered planting dates of Brassica rapa families with known flowering times, creating populations in which age at flowering (i.e., flowering time genotype) and Julian date of flowering (i.e., flowering time environment) were positively, negatively, or uncorrelated. Genetic paternity analysis revealed that male fitness was not strongly influenced by seasonal environmental changes. Instead, when age and date were uncorrelated, selection through male fitness strongly favored young age at flowering. Strategic sampling offspring for paternity analysis rejected covariance between sire age at flowering and dam quality as the cause of this selection. Results instead suggest a negative association between age at flowering and pollen competitive ability. The manipulation also revealed that, at least in B. rapa, the often‐observed correlation between flowering time and flowering duration is environmental, not genetic, in origin.     

Microbial effects on plant phenology and fitness

Plant development and the timing of developmental events (phenology) are tightly coupled with plant fitness. A variety of internal and external factors determine the timing and fitness consequences of these life-history transitions. Microbes interact with plants throughout their life history and impact host phenology. This review summarizes current mechanistic and theoretical knowledge surrounding microbe-driven changes in plant phenology. Overall, there are examples of microbes impacting every phenological transition. While most studies have focused on flowering time, microbial effects remain important for host survival and fitness across all phenological phases. Microbe-mediated changes in nutrient acquisition and phytohormone signaling can release plants from stressful conditions and alter plant stress responses inducing shifts in developmental events. The frequency and direction of phenological effects appear to be partly determined by the lifestyle and the underlying nature of a plant–microbe interaction (i.e., mutualistic or pathogenic), in addition to the taxonomic group of the microbe (fungi vs. bacteria). Finally, we highlight biases, gaps in knowledge, and future directions. This biotic source of plasticity for plant adaptation will serve an important role in sustaining plant biodiversity and managing agriculture under the pressures of climate change.     

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.     

Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks

The relationship between ecological variation and microbial genetic composition is critical to understanding microbial influence on community and ecosystem function. In glasshouse trials using nine native legume species and 40 rhizobial strains, we find that bacterial rRNA phylotype accounts for 68% of amoung isolate variability in symbiotic effectiveness and 79% of host specificity in growth response. We also find that rhizobial phylotype diversity and composition of soils collected from a geographical breadth of sites explains the growth responses of two acacia species. Positive soil microbial feedback between the two acacia hosts was largely driven by changes in diversity of rhizobia. Greater rhizobial diversity accumulated in association with the less responsive host species, Acacia salicina, and negatively affected the growth of the more responsive Acacia stenophylla. Together, this work demonstrates correspondence of phylotype with microbial function, and demonstrates that the dynamics of rhizobia on host species can feed back on plant population performance.     

Simultaneous selection on vegetative and reproductive phenology in a perennial herb

The timing of different life‐history events is often correlated, and selection might only rarely be exerted independently on the timing of a single event. In plants, phenotypic selection has often been shown to favor earlier flowering. However, little is known about to what extent this selection acts directly versus indirectly via vegetative phenology, and if selection on the two traits is correlational. We estimated direct, indirect, and correlational phenotypic selection on vegetative and reproductive phenology over 3 years for flowering individuals of the perennial herb Lathyrus vernus. Direct selection favored earlier flowering and shorter timespans between leaf‐out and flowering in all years. However, early flowering was associated with early leaf‐out, and the direction of selection on leaf‐out day varied among years. As a result, selection on leaf‐out weakened selection for early flowering in one of the study years. We found no evidence of correlational selection. Our results highlight the importance of including temporally correlated traits when exploring selection on the phenology of seasonal events.     

Toward a synthetic understanding of the role of phenology in ecology and evolution

Phenology affects nearly all aspects of ecology and evolution. Virtually all biological phenomena—from individual physiology to interspecific relationships to global nutrient fluxes—have annual cycles and are influenced by the timing of abiotic events. Recent years have seen a surge of interest in this topic, as an increasing number of studies document phenological responses to climate change. Much recent research has addressed the genetic controls on phenology, modelling techniques and ecosystem-level and evolutionary consequences of phenological change. To date, however, these efforts have tended to proceed independently. Here, we bring together some of these disparate lines of inquiry to clarify vocabulary, facilitate comparisons among habitat types and promote the integration of ideas and methodologies across different disciplines and scales. We discuss the relationship between phenology and life history, the distinction between organismal- and population-level perspectives on phenology and the influence of phenology on evolutionary processes, communities and ecosystems. Future work should focus on linking ecological and physiological aspects of phenology, understanding the demographic effects of phenological change and explicitly accounting for seasonality and phenology in forecasts of ecological and evolutionary responses to climate change.     

模式植物拟南芥开花时间分子调控研究进展

植物从营养生长到生殖生长的转变是开花发育的关键,在合适的时间开花对植物的生长和繁衍极为重要,植物开花时间的调控对农业生产发展意义重大。植物开花是由遗传因子和环境因子协同调节的一个复杂过程。近年来,对不同植物开花调控的研究,特别是对模式植物拟南芥（Arabidopsis thaliana（L.） Heynh.）的开花调控研究取得了显著进展,已探明开花时间分子调控的6条主要途径分别是光周期途径、春化途径、自主途径、温度途径、赤霉素途径和年龄途径。各遗传调控途径既相互独立又相互联系,构成一个复杂的开花调控网络。本文综述了模式植物拟南芥开花时间调控分子机制相关研究的最新进展,并对未来的研究进行了展望。     

Phenological mismatch drives selection on elevation,but not on slope,of breeding time plasticity in a wild songbird

Phenotypic plasticity is an important mechanism for populations to respond to fluctuating environments, yet may be insufficient to adapt to a directionally changing environment. To study whether plasticity can evolve under current climate change, we quantified selection and genetic variation in both the elevation (RN_E) and slope (RN_S) of the breeding time reaction norm in a long‐term (1973–2016) study population of great tits (Parus major). The optimal RN_E (the caterpillar biomass peak date regressed against the temperature used as cue by great tits) changed over time, whereas the optimal RN_S did not. Concordantly, we found strong directional selection on RN_E, but not RN_S, of egg‐laying date in the second third of the study period; this selection subsequently waned, potentially due to increased between‐year variability in optimal laying dates. We found individual and additive genetic variation in RN_E but, contrary to previous studies on our population, not in RN_S. The predicted and observed evolutionary change in RN_E was, however, marginal, due to low heritability and the sex limitation of laying date. We conclude that adaptation to climate change can only occur via micro‐evolution of RN_E, but this will necessarily be slow and potentially hampered by increased variability in phenotypic optima.     

Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts

The timing of the snowmelt is a crucial factor in determining the phenological schedule of alpine plants. A long-term monitoring of snowmelt regimes in a Japanese alpine area revealed that the onset of the snowmelt season has been accelerated during the last 17 years in early snowmelt sites but that such a trend has not been detected in late snowmelt sites. This indicates that the global warming effect on the snowmelt pattern may be site-specific. The flowering phenology of fellfield plants in an exposed wind-blown habitat was consistent between an unusually warm year (1998) and a normal year (2001). In contrast, the flowering occurrence of snowbed plants varied greatly between the years depending on the snowmelt time. There was a large number of flowering species in the fellfield community from mid- to late to late June and from mid- to late July. The flowering peak of an early-melt snowbed plant community was in the middle of the flowering season and that of a late-melt snowbed community was in the early flowering season. These habitat-specific phenological patterns were consistent between 1998 and 2001. The effects of the variation in flowering timing on seed-set success were evaluated for an entomophilous snowbed herb, Peucedanum multivittatum, along the snowmelt gradient during a 5-year period. When flowering occurred prior to early August, mean temperature during the flowering season positively influenced the seed set. When flowering occurred later than early August, however, the plants enjoyed high seed-set success irrespective of temperature conditions if frost damage was absent. These observations are probably explained based on the availability of pollinators, which depends not only on ambient temperature but also on seasonal progress. These results suggest that the effects of climate change on biological interaction may vary depending on the specific habitat in the alpine ecosystem in which diverse snowmelt patterns create complicated seasonality for plants within a very localized area.     

Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping

To identify the ecological and genetic mechanisms of local adaptation requires estimating selection on traits, identifying their genetic basis, and evaluating whether divergence in adaptive traits is due to conditional neutrality or genetic trade‐offs. To this end, we conducted field experiments for three years using recombinant inbred lines (RILs) derived from two ecotypes of Arabidopsis thaliana (Italy, Sweden), and at each parental site examined selection on flowering time and mapped quantitative trait loci (QTL). There was strong selection for early flowering in Italy, but weak selection in Sweden. Eleven distinct flowering time QTL were detected, and for each the Italian genotype caused earlier flowering. Twenty‐seven candidate genes were identified, two of which (FLC and VIN3) appear under major flowering time QTL in Italy. Seven of eight QTL in Italy with narrow credible intervals colocalized with previously reported fitness QTL, in comparison to three of four in Sweden. The results demonstrate that the magnitude of selection on flowering time differs strikingly between our study populations, that the genetic basis of flowering time variation is multigenic with some QTL of large effect, and suggest that divergence in flowering time between ecotypes is due mainly to conditional neutrality.     

Strong selection on mandible and nest features in a carpenter bee that nests in two sympatric host plants

Host plants are used by herbivorous insects as feeding or nesting resources. In wood‐boring insects, host plants features may impose selective forces leading to phenotypic differentiation on traits related to nest construction. Carpenter bees build their nests in dead stems or dry twigs of shrubs and trees; thus, mandibles are essential for the nesting process, and the nest is required for egg laying and offspring survival. We explored the shape and intensity of natural selection on phenotypic variation on three size measures of the bees (intertegular width, wing length, and mandible area) and two nest architecture measures (tunnel length and diameter) on bees using the native species Chusquea quila (Poaceae), and the alloctonous species Rubus ulmifolius (Rosaceae), in central Chile. Our results showed significant and positive linear selection gradients for tunnel length on both hosts, indicating that bees building long nests have more offspring. Bees with broader mandibles show greater fitness on C. quila but not on R. ulmifolius. Considering that C. quila represents a selective force on mandible area, we hypothesized a high adaptive value of this trait, resulting in higher fitness values when nesting on this host, despite its wood is denser and hence more difficult to be bored.     

Rainfall and flowering synchrony in a tropical shrub: Variable selection on the flowering time ofErythroxylum havanense

Summary We tested the adaptive significance of flowering synchrony by means of a quantitative analysis of selection and by flowering induction experiments with the deciduous shrubErythroxylum havanense. Temporal schedules of flower and fruit production were determined for a local population (in three sites) in a Mexican seasonal forest for 2 years (1987–1988). The consequences of natural variation in flowering time (flowering initiation day) on maternal reproductive success (fecundity) were evaluated. We observed high levels of inter- and intraindividual flowering synchrony in 1987, but not in 1988 and this contrast was related to differences in rainfall patterns between the two years. A significant proportion (15.4%) of the phenotypic variation in flowering initiation day was accounted for by environmental variance. The expression of phenotypic variance of flowering time and, consequently, the opportunity for selection to act, are controlled by annual variation in rainfall. Despite the between-year difference in flowering synchrony, we detected a relatively intense directional selection on flowering initiation day in both years, but selection coefficients were of opposite sign (standardized directional gradients were –0.326 and 0.333 for 1987 and 1988, respectively). For both years there was a significant relationship between individual relative fitness and the number of neighbouring flowering plants in a given day, suggesting positive frequency-dependent selection.     

Phenology and phenotypic natural selection on the flowering time of a deceit-pollinated tropical orchid, Myrmecophila christinae

BACKGROUND AND AIMS: Flowering phenology is described and the effect of flowering time on pollination success is evaluated in the deceit-pollinated tropical orchid, Myrmecophila christinae. It was expected that, due to this species' deceit pollination strategy and low observed pollinator visit rate, there would be a higher probability of natural selection events favouring individuals flowering away from the population flowering peak. METHODS: The study covers two consecutive years and four populations of M. christinae located along the north coast of the Yucatán Peninsula. For phenological and pollination success data, a total of 110 individuals were monitored weekly in 1998, and 83 individuals in 1999, during all the flowering and fruiting season. KEY RESULTS: The results showed significant differences in the probability of donating and receiving pollen throughout the flowering season. The probability of receiving or donating pollen increased the further an individual flowering was from the flowering peak. Regression analysis showed directional and disruptive phenotypic natural selection gradients, suggesting the presence of selection events unfavourable to flowering during flowering peak, for both male success (pollen removal) and female success (fruit production). However, the intensity and significance of the natural selection events varied between populations from year to year. The variation between seasons and populations was apparently due to variations in the density of reproductive individuals in each population and each season. CONCLUSIONS: As in other deceit-pollinated orchids, natural selection in M. christinae favours individuals flowering early or late in relation to population peak flowering. However, results also suggested a fluctuating regime of selective events act on flowering time of M. christinae.