Behavioural Thermoregulation of Flowers via Petal Movement.

Widely documented in animals, behavioural thermoregulation mitigates negative impacts of climate change. Plants experience especially strong thermal variability but evidence for plant behavioural thermoregulation is limited. Along a montane elevation gradient, Argentina anserina flowers warm more in alpine populations than at lower elevation. We linked floral temperature with phenotypes to identify warming mechanisms and documented petal movement and pollinator visitation using time-lapse cameras. High elevation flowers were more cupped, focused light deeper within flowers and were more responsive to air temperature than low; cupping when cold and flattening when warm. At high elevation, a 20° increase in petal angle resulted in a 0.46°C increase in warming. Warming increased pollinator visitation, especially under cooler high elevation temperatures. A plasticity study revealed constitutive elevational differences in petal cupping and stronger temperature-induced floral plasticity in high elevation populations. Thus, plant populations have evolved different behavioural responses to temperature driving differences in thermoregulatory capacity.

Nectar and floral morphology differ in evolutionary potential in novel pollination environments.

Plants can evolve rapidly after pollinator changes, but the response of different floral traits to novel selection can vary. Floral morphology is often expected to show high integration to maintain pollination accuracy, while nectar traits can be more environmentally sensitive. The relative role of genetic correlations and phenotypic plasticity (PP) in floral evolution remains unclear, particularly for nectar traits, and can be studied in the context of recent pollinator changes. Digitalis purpurea shows rapid recent evolution of corolla morphology but not nectar traits following a range expansion with hummingbirds added as pollinators. We use this species to compare PP, heritability, evolvability and integration of floral morphology and nectar in a common garden. Morphological traits showed higher heritability than nectar traits, and the proximal section of the corolla, which regulates access to nectar and underwent rapid change in introduced populations, presented lower integration than the rest of the floral phenotype. Nectar was more plastic than morphology, driven by highly plastic sugar concentration. Nectar production rate showed high potential to respond to selection. These results explain the differential rapid evolution of floral traits previously observed in this species and show how intrafloral modularity determines variable evolutionary potential in morphological and nectar traits.

Parallel evolution of morphological and genomic selfing syndromes accompany the breakdown of heterostyly.

Evolutionary transitions from outcrossing to selfing in flowering plants have convergent morphological and genomic signatures and can involve parallel evolution within related lineages. Adaptive evolution of morphological traits is often assumed to evolve faster than nonadaptive features of the genomic selfing syndrome. We investigated phenotypic and genomic changes associated with transitions from distyly to homostyly in the Primula oreodoxa complex. We determined whether the transition to selfing occurred more than once and investigated stages in the evolution of morphological and genomic selfing syndromes using 22 floral traits and both nuclear and plastid genomic data from 25 populations. Two independent transitions were detected representing an earlier and a more recently derived selfing lineage. The older lineage exhibited classic features of the morphological and genomic selfing syndrome. Although features of both selfing syndromes were less developed in the younger selfing lineage, they exhibited parallel development with the older selfing lineage. This finding contrasts with the prediction that some genomic changes should lag behind adaptive changes to morphological traits. Our findings highlight the value of comparative studies on the timing and extent of transitions from outcrossing to selfing between related lineages for investigating the tempo of morphological and molecular evolution.

High floral disparity without pollinator shifts in buzz-bee-pollinated Melastomataceae.

Shifts among functional pollinator groups are commonly regarded as sources of floral morphological diversity (disparity) through the formation of distinct pollination syndromes. While pollination syndromes may be used for predicting pollinators, their predictive accuracy remains debated, and they are rarely used to test whether floral disparity is indeed associated with pollinator shifts. We apply classification models trained and validated on 44 functional floral traits across 252 species with empirical pollinator observations and then use the validated models to predict pollinators for 159 species lacking observations. In addition, we employ multivariate statistics and phylogenetic comparative analyses to test whether pollinator shifts are the main source of floral disparity in Melastomataceae. We find strong support for four well-differentiated pollination syndromes ('buzz-bee', 'nectar-foraging vertebrate', 'food-body-foraging vertebrate', 'generalist'). While pollinator shifts add significantly to floral disparity, we find that the most species-rich 'buzz-bee' pollination syndrome is most disparate, indicating that high floral disparity may evolve without pollinator shifts. Also, relatively species-poor clades and geographic areas contributed substantially to total disparity. Finally, our results show that machine-learning approaches are a powerful tool for evaluating the predictive accuracy of the pollination syndrome concept as well as for predicting pollinators where observations are missing.

Angiosperm flowers reached their highest morphological diversity early in their evolutionary history.

Flowers are the complex and highly diverse reproductive structures of angiosperms. Because of their role in sexual reproduction, the evolution of flowers is tightly linked to angiosperm speciation and diversification. Accordingly, the quantification of floral morphological diversity (disparity) among angiosperm subgroups and through time may give important insights into the evolutionary history of angiosperms as a whole. Based on a comprehensive dataset focusing on 30 characters describing floral structure across angiosperms, we used 1201 extant and 121 fossil flowers to measure floral disparity and explore patterns of floral evolution through time and across lineages. We found that angiosperms reached their highest floral disparity in the Early Cretaceous. However, decreasing disparity toward the present likely has not precluded the innovation of other complex traits at other morphological levels, which likely played a key role in the outstanding angiosperm species richness. Angiosperms occupy specific regions of the theoretical morphospace, indicating that only a portion of the possible floral trait combinations is observed in nature. The ANA grade, the magnoliids, and the early-eudicot grade occupy large areas of the morphospace (higher disparity), whereas nested groups occupy narrower regions (lower disparity).

How the switch to hummingbird pollination has greatly contributed to our understanding of evolutionary processes.

The evolutionary switch to hummingbird pollination exemplifies complex adaptation, requiring evolutionary change in multiple component traits. Despite this complexity, diverse lineages have converged on hummingbird-adapted flowers on a relatively short evolutionary timescale. Here, I review how features of the genetic basis of adaptation contribute to this remarkable evolutionary lability. Large-effect substitutions, large mutational targets for adaptation, adaptive introgression, and concentrated architecture all contribute to the origin and maintenance of hummingbird-adapted flowers. The genetic features of adaptation are likely shaped by the ecological and geographic context of the switch to hummingbird pollination, with implications for future evolutionary trajectories.

The effect of global change on the expression and evolution of floral traits.

BACKGROUND: Pollinators impose strong selection on floral traits. Indeed, pollinator syndromes are the result of these strong selective forces, but other abiotic and biotic agents also drive the evolution of floral traits and influence plant reproduction. Global change is expected to have widespread effects on biotic and abiotic systems resulting in novel selection on floral traits under future conditions. SCOPE: Global change has depressed pollinator abundance and altered abiotic conditions, thereby exposing flowering plant species to novel suites of selective pressures. Here we consider how biotic and abiotic factors interact to shape the expression and evolution of various floral characteristics (the targets of selection), including floral size, color, physiology, reward quantity and quality, and longevity amongst other traits. We examine cases in which selection imposed by climatic factors conflicts with pollinator-mediated selection. Additionally, we explore how floral traits respond to environmental changes through phenotypic plasticity and how that can alter plant fecundity. In this review, we evaluate how global change may shift the expression and evolution of floral phenotypes. CONCLUSIONS: Floral traits evolve in response to multiple interacting agents of selection. Different agents can sometimes exert conflicting selection. For example, pollinators often prefer large flowers, but drought stress can favor the evolution of smaller flowers, and the size of floral organs can evolve as a trade-off between selection mediated by these opposing actors. Nevertheless, few studies have factorially manipulated abiotic and biotic agents of selection to disentangle their relative strengths and directions of selection. The literature has more often evaluated plastic responses of floral traits to stressors than it has considered how abiotic factors alter selection on these traits. Furthermore, global change will likely alter the selective landscape through changes in the abundance and community compositions of mutualists and antagonists and novel abiotic conditions. We encourage future work to consider a more holistic model of floral evolution, which will enable more robust predictions about floral evolution and plant reproduction as global change progresses.

Harvesting pollen with vibrations: towards an integrative understanding of the proximate and ultimate reasons for buzz pollination.

Buzz pollination, a type of interaction in which bees use vibrations to extract pollen from certain kinds of flowers, captures a close relationship between thousands of bee and plant species. In the last 120 years, studies of buzz pollination have contributed to our understanding of the natural history of buzz pollination, and basic properties of the vibrations produced by bees and applied to flowers in model systems. Yet, much remains to be done to establish its adaptive significance and the ecological and evolutionary dynamics of buzz pollination across diverse plant and bee systems. Here, we review for bees and plants the proximate (mechanism and ontogeny) and ultimate (adaptive significance and evolution) explanations for buzz pollination, focusing especially on integrating across these levels to synthesize and identify prominent gaps in our knowledge. Throughout, we highlight new technical and modelling approaches and the importance of considering morphology, biomechanics and behaviour in shaping our understanding of the adaptive significance of buzz pollination. We end by discussing the ecological context of buzz pollination and how a multilevel perspective can contribute to explain the proximate and evolutionary reasons for this ancient bee-plant interaction.

Zygomorphic flowers last longer: the evolution of floral symmetry and floral longevity.

Floral longevity, the length of time a flower remains open and functional, is a phylogenetically conserved trait that balances floral costs against the rate at which flowers are pollinated. Floral symmetry has long been considered a key trait in floral evolution. Although zygomorphic (bilaterally symmetric) flowers typically receive fewer floral visitors than actinomorphic (radially symmetric) flowers, it is yet to be determined whether this could be associated with longer floral longevity. Using newly collected field data combined with data from the literature on 1452 species in 168 families, we assess whether floral longevity covaries with floral symmetry in a phylogenetic framework. We find that zygomorphic flowers last on average 1.1 days longer than actinomorphic flowers, a 26.5% increase in longevity, with considerable variation across both groups. Our results provide a basis to discuss the ecological and evolutionary costs of zygomorphy for plants. Despite these costs, zygomorphy has evolved numerous times throughout angiosperm history, and we discuss which rewards may outweigh the costs of slower pollination in zygomorphic flowers.

A design principle for floral organ number and arrangement in flowers with bilateral symmetry.

The bilateral symmetry of flowers is a striking morphological achievement during floral evolution, providing high adaptation potential for pollinators. The symmetry can appear when floral organ primordia developmentally initiate. Primordia initiation at the ventral and dorsal sides of the floral bud is differentially regulated by several factors, including external organs of the flower and CYCLOIDEA (CYC) gene homologues, which are expressed asymmetrically on the dorso-ventral axis. It remains unclear how these factors control the diversity in the number and bilateral arrangement of floral organs. Here, we propose a mathematical model demonstrating that the relative strength of the dorsal-to-ventral inhibitions and the size of the floral stem cell region (meristem) determines the number and positions of the sepal and petal primordia. The simulations reproduced the diversity of monocots and eudicots, including snapdragon Antirrhinum majus and its cyc mutant, with respect to organ number, arrangement and initiation patterns, which were dependent on the inhibition strength. These theoretical results suggest that diversity in floral symmetry is primarily regulated by the dorso-ventral inhibitory field and meristem size during developmental evolution.

Quantitative genetic analysis of floral traits shows current limits but potential evolution in the wild.

The vast variation in floral traits across angiosperms is often interpreted as the result of adaptation to pollinators. However, studies in wild populations often find no evidence of pollinator-mediated selection on flowers. Evolutionary theory predicts this could be the outcome of periods of stasis under stable conditions, followed by shorter periods of pollinator change that provide selection for innovative phenotypes. We asked if periods of stasis are caused by stabilizing selection, absence of other forms of selection or by low trait ability to respond even if selection is present. We studied a plant predominantly pollinated by one bee species across its range. We measured heritability and evolvability of traits, using genome-wide relatedness in a large wild population, and combined this with estimates of selection on the same individuals. We found evidence for both stabilizing selection and low trait heritability as potential explanations for stasis in flowers. The area of the standard petal is under stabilizing selection, but the variability is not heritable. A separate trait, floral weight, presents high heritability, but is not currently under selection. We show how a simple pollination environment coincides with the absence of current prerequisites for adaptive evolutionary change, while heritable variation remains to respond to future selection pressures.

All's well that ends well: the timing of floral meristem termination.

Floral meristem termination (FMT) represents one of the defining features of a floral meristem relative to a vegetative meristem. Timing of FMT is a major determinant of the total number of organs in a flower, and canalization toward relatively rapid FMT is considered to have been a major force in shaping angiosperm evolution. For decades, investigation of FMT has been focused on model systems that only produce four whorls of organs in a flower, while little is known about the molecular basis that underlies nature variation in the timing of FMT. Here, we hypothesize on how known pathways could have been modified to generate variation in FMT and explain how developing new model systems will help to deepen our understanding of the genetic control and evolution of FMT.

Soil water and nutrient availability interactively modify pollinator-mediated directional and correlational selection on floral display.

The individual and combined effects of abiotic factors on pollinator-mediated selection on floral traits are not well documented. To examine potential interactive effects of water and nutrient availability on pollinator-mediated selection on three floral display traits of Primula tibetica, we manipulated pollination and nutrient availability in a factorial experiment, conducted at two common garden sites with different soil water content (natural vs addition). We found that both water and nutrient availability affected floral trait expression in P. tibetica and that hand pollination increased seed production most when both nutrient content and water content were high, indicating joint pollen and resource limitation. We documented selection on all floral traits, and pollinators contributed to directional and correlational selection on plant height and number of flowers. Soil water and nutrient availability interactively influenced the strength of both pollinator-mediated directional and correlational selection, with significant selection observed when nutrient or water availability was high, but not when none or both were added. The results suggest that resource limitation constrains the response of P. tibetica to among-individual variation in pollen receipt, that addition of nutrients or water leads to pollinator-mediated selection and that effects of the two abiotic factors are nonadditive.

Development differs between independently evolved staminode whorls in the same flower.

PREMISE: Staminodes are commonly studied in hermaphroditic flowers, in which a fraction of the androecium evolves into infertile structures, but few studies have addressed the evolution of staminodes as they occur through the loss of stamen function in carpellate flowers. Plants of Paronychia (Caryophyllaceae) are monoecious with hermaphroditic flowers with one staminodial whorl, except for the dioecious P. chartacea and P. minima. Dioecious species have carpellate flowers that evolved an additional whorl of staminodes, providing an exceptional opportunity to study a second origin of staminodes in the same flower. METHODS: Using scanning electron microscopy, we observed the development of carpellate and staminate flowers to determine whether the developmental pathway of the staminodes in hermaphroditic flowers was co-opted during the evolutionary transition to unisexual flowers. RESULTS: In carpellate flowers, antesepalous staminodes initiate as sterile anthers that develop similar to functioning stamens, but arrest before full development, leaving a rudimentary anther with lateral lobes that correspond to thecae. After antesepalous staminodes arrest, alternisepalous staminodes initiate as structures that correspond with filaments, as they do in staminate and hermaphroditic flowers. CONCLUSIONS: The second origin of staminodes in carpellate flowers evolved using a different developmental pathway than what had previously evolved in the alternisepalous whorl. The two androecial whorls in the same flowers are serialogous as members of the androecium, but are paralogous as staminodes on the basis of structural and developmental differences.

The role of petal transpiration in floral humidity generation.

MAIN CONCLUSION: Using petrolatum gel as an antitranspirant on the flowers of California poppy and giant bindweed, we show that transpiration provides a large contribution to floral humidity generation. Floral humidity, an area of elevated humidity in the headspace of flowers, is believed to be produced predominantly through a combination of evaporation of liquid nectar and transpirational water loss from the flower. However, the role of transpiration in floral humidity generation has not been directly tested and is largely inferred by continued humidity production when nectar is removed from flowers. We test whether transpiration contributes to the floral humidity generation of two species previously identified to produce elevated floral humidity, Calystegia silvatica and Eschscholzia californica. Floral humidity production of flowers that underwent an antitranspirant treatment, petrolatum gel which blocks transpiration from treated tissues, is compared to flowers that did not receive such treatments. Gel treatments reduced floral humidity production to approximately a third of that produced by untreated flowers in C. silvatica, and half of that in E. californica. This confirms the previously untested inferences that transpiration has a large contribution to floral humidity generation and that this contribution may vary between species.

Disruptive selection via pollinators and seed predators on the height of flowers on a wind-dispersed alpine herb.

PREMISE: Floral stalk height is known to affect seed dispersal of wind-dispersed grassland species, but it may also affect the attractiveness of flowers and fruits of animal-pollinated and animal-dispersed plants. Stalk height may thus be responsive to selection via interactions with both mutualist pollinators and seed dispersers, but also antagonist florivores and seed predators. In this study, we aimed to determine the effect of pollinators and seed predators on selection on floral stalk height in the insect-pollinated and wind-dispersed, alpine, andromonoecious herb Pulsatilla alpina, whose flowers also vary in their sex allocation and thus in the resources available to both mutualists and antagonists. METHODS: We measured the resource status of individuals in terms of their size and the height of the vegetation surrounding plants of P. alpina at 11 sites. In one population, we recorded floral stalk height over an entire growing season and investigated its association with floral morphology and floral sex allocation (pistil and stamen number) and used leaf-removal manipulations to assess the effect of herbivory on floral stalk height. Finally, in four populations, we quantified phenotypic selection on floral stalk height in four female components of reproductive success before seed dispersal. RESULTS: Stalk height was positively associated with female allocation of the respective flower, the resource status of the individual, and the height of the surrounding vegetation, and negatively affected by leaf removal. Our results point to disruptive selection on stalk height in terms of both selection differentials and selection gradients for fertilization, seed predation, and seed maturation rates and to positive selection on stalk height in terms of a selection differential for mature seed number. CONCLUSIONS: Stalk height of P. alpina is a costly trait that affects female reproductive success via interactions with both mutualists and antagonists. We discuss the interplay between the resource status and selection imposed on female reproductive success and its likely role in the evolution of sex-allocation strategies, especially andromonoecy.

Low bee visitation rates explain pollinator shifts to vertebrates in tropical mountains.

Evolutionary shifts from bee to vertebrate pollination are common in tropical mountains. Reduction in bee pollination efficiency under adverse montane weather conditions was proposed to drive these shifts. Although pollinator shifts are central to the evolution and diversification of angiosperms, we lack experimental evidence of the ecological processes underlying such shifts. Here, we combine phylogenetic and distributional data for 138 species of the Neotropical plant tribe Merianieae (Melastomataceae) with pollinator observations of 11 and field pollination experiments of six species to test whether the mountain environment may indeed drive such shifts. We demonstrate that shifts from bee to vertebrate pollination coincided with occurrence at high elevations. We show that vertebrates were highly efficient pollinators even under the harsh environmental conditions of tropical mountains, whereas bee pollination efficiency was lowered significantly through reductions in flower visitation rates. Furthermore, we show that pollinator shifts in Merianieae coincided with the final phases of the Andean uplift and were contingent on adaptive floral trait changes to alternative rewards and mechanisms facilitating pollen dispersal. Our results provide evidence that abiotic environmental conditions (i.e. mountain climate) may indeed reduce the efficiency of a plant clade's ancestral pollinator group and correlate with shifts to more efficient new pollinators.

A test of Sensory Drive in plant-pollinator interactions: heterogeneity in the signalling environment shapes pollinator preference for a floral visual signal.

Sensory Drive predicts that habitat-dependent signal transmission and perception explain the diversification of communication signals. Whether Sensory Drive shapes floral evolution remains untested in nature. Pollinators of Argentina anserina prefer small ultraviolet (UV)-absorbing floral guides at low elevation but larger guides at high. However, mechanisms underlying differential preference are unclear. High elevation populations experience elevated UV irradiance and frequently flower against bare substrates rather than foliage, potentially impacting signal transmission and perception. At high and low elevation extremes, we experimentally tested the effects of UV light (ambient vs reduced) and floral backgrounds (foliage vs bare) on pollinator choice for UV guide size. We examined how different signalling environments shaped pollinator-perceived flower colour using visual system models. At high elevation, pollinators preferred locally common large UV guides under ambient UV, but lacked preference under reduced UV. Flies preferred large guides only against bare substrate, the common high elevation background. Ambient UV amplified contrast of large UV guides with floral backgrounds, and flowers contrasted more with bare ground than foliage. Results support that local signalling conditions contribute to pollinator preference for a floral visual signal, a key tenet of Sensory Drive. Components of Sensory Drive could shape floral signal evolution in other plants spanning heterogeneous signalling environments.

Floral development and vasculature in Eriocaulon (Eriocaulaceae) provide insights into the evolution of Poales.

BACKGROUND AND AIMS: Floral developmental studies are crucial for understanding the evolution of floral structures and sexual systems in angiosperms. Within the monocot order Poales, both subfamilies of Eriocaulaceae have unisexual flowers bearing unusual nectaries. Few previous studies have investigated floral development in subfamily Eriocauloideae, which includes the large, diverse and widespread genus Eriocaulon. To understand floral variation and the evolution of the androecium, gynoecium and floral nectaries of Eriocaulaceae, we analysed floral development and vasculature in Eriocaulon and compared it with that of subfamily Paepalanthoideae and the related family Xyridaceae in a phylogenetic context. METHODS: Thirteen species of Eriocaulon were studied. Developmental analysis was carried out using scanning electron microscopy, and vasculature analysis was carried out using light microscopy. Fresh material was also analysed using scanning electron microscopy with a cryo function. Character evolution was reconstructed over well-resolved phylogenies. KEY RESULTS: Perianth reductions can occur due to delayed development that can also result in loss of the vascular bundles of the median sepals. Nectariferous petal glands cease development and remain vestigial in some species. In staminate flowers, the inner stamens can emerge before the outer ones, and carpels are transformed into nectariferous carpellodes. In pistillate flowers, stamens are reduced to staminodes and the gynoecium has dorsal stigmas. CONCLUSIONS: Floral morphology is highly diverse in Eriocaulon, as a result of fusion, reduction or loss of perianth parts. The nectariferous carpellodes of staminate flowers originated first in the ancestor of Eriocaulaceae; petal glands and nectariferous branches of pistillate flowers originated independently in Eriocaulaceae through transfer of function. We present a hypothesis of floral evolution for the family, illustrating a shift from bisexuality to unisexuality and the evolution of nectaries in a complex monocot family, which can contribute to future studies on reproductive biology and floral evolution in other groups.

Evolution of apetaly in the cosmopolitan genus Stellaria.

PREMISE: Apetaly is widespread across distantly related lineages of flowering plants and is associated with abiotic (or self-) pollination. It is particularly prevalent in the carnation family, and the cosmopolitan genus Stellaria contains many lineages that are hypothesized to have lost petals from showy petalous ancestors. But the pollination biology of apetalous species of Stellaria remains unclear. METHODS: Using a substantial species-level sampling (~92% of known taxonomic diversity), we describe the pattern of petal evolution within Stellaria using ancestral character state reconstructions. To help shed light on the reproductive biology of apetalous Stellaria, we conducted a field experiment at an alpine tundra site in the southern Rocky Mountains to test whether an apetalous species (S. irrigua) exhibits higher levels of selfing than a sympatric, showy petalous congener (S. longipes). RESULTS: Analyses indicated that the ancestor of Stellaria was likely showy petalous and that repeated, parallel reductions of petals occurred in clades across much of the world, with uncommon reversal back to showy petals. Field experiments supported high rates of selfing in the apetalous species and high rates of outcrossing in the petalous species. CONCLUSIONS: Petal loss is rampant across major clades of Stellaria and is potentially linked with self-pollination worldwide. Self-pollination occurs within the buds in S. irrigua, and high propensities for this and other forms of selfing known in many other taxa of arctic-alpine habitats may reflect erratic availability of pollinators.