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.
METHODS: 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.

Pollen plays a key role in plant reproductive biology. Despite the long history of research on pollen and pollination, recent advances in pollen-tracking methods and statistical approaches to linking plant phenotype, pollination performance, and reproductive fitness yield a steady flow of exciting new insights. In this introduction to the Special Issue \"Pollen as the Link Between Phenotype and Fitness,\" we start by describing a general conceptual model linking functional classes of floral phenotypic traits to pollination-related performance metrics and reproductive fitness. We use this model as a framework for synthesizing the relevant literature, highlighting the studies included in the Special Issue, and identifying gaps in our understanding and opportunities for further development of the field. The papers that follow in this Special Issue provide new insights into the relationships between pollen production, presentation, flower morphology, and pollination performance (e.g., pollen deposition onto stigmas), the role of pollinators in pollen transfer, and the consequences of heterospecific pollen deposition. Several of the studies demonstrate exciting experimental and analytical approaches that should pave the way for continued work addressing the intriguing role of pollen in linking plant phenotypes to reproductive fitness.

AbstractIn animal-pollinated plants, the growth environment and pollination environment are two important agents of natural selection. However, their simultaneous effects on plant speciation remain underexplored. Here, we report a theoretical finding that if plants\' local adaptation to the growth environment increases their floral rewards for pollinators, it can strongly facilitate ecological speciation in plants. We consider two evolving plant traits, vegetative and floral signal traits, in a population genetic model for two plant populations under divergent selection from different growth environments. The vegetative trait determines plants\' local adaptation. Locally adapted plants reward pollinators better than maladapted plants. By associative learning, pollinators acquire learned preferences for floral signal traits expressed by better-rewarding plants. If pollinators\' learned preferences become divergent between populations, floral signal divergence occurs and plants develop genetic associations between vegetative and floral signal traits, leading to ecological speciation via a two-allele mechanism. Interestingly, speciation is contingent on whether novel floral signal variants arise before or after plant populations become locally adapted to the growth environment. Our results suggest that simultaneous selection from growth and pollination environments might be important for the ecological speciation of animal-pollinated plants.

Floral traits are frequently under pollinator-mediated selection, especially in taxa subject to strong pollen-limitation, such as those reliant on pollinators. However, antagonists can be agents of selection on floral traits as well. The causes of selection acting on spring ephemerals are understudied though these species can experience particularly strong pollen-limitation. I examined pollinator- and antagonist-mediated selection in a narrowly endemic spring ephemeral, Trillium discolor.
I measured pollen limitation in T. discolor across two years and evaluated its breeding system. I compared selection on floral traits (display height, petal size, petal color, flowering time) between open-pollinated, and pollen-supplemented plants to measure the strength and mode of pollinator-mediated selection. I assessed whether natural levels of antagonism impacted selection on floral traits.
Trillium discolor was self-incompatible and experienced pollen limitation in both years of the study. Pollinators exerted negative disruptive selection on display height and petals size. In one year, pollinator-mediated selection favored lighter petals but in the second year pollinators favored darker petals. Antagonist damage did not alter selection on floral traits.
Results demonstrate that pollinators mediate the strength and mode of selection on floral traits in T. discolor. Interannual variation in the strength, mode, and direction of pollinator-mediated selection on floral traits could be important for maintaining of floral diversity in this system. Observed levels of antagonism were weak agents of selection on floral traits.

[This corrects the article DOI: 10.3389/fpls.2022.807689.].

Abiotic environmental factors are predicted to affect plant traits and the intensity of plant-pollinator interactions. However, knowledge of their potential effects on pollinator-mediated selection on floral traits is still limited. We separately estimated the effects of soil water (two sites with different soil water contents) and N-P-K nutrient availability (different levels of nutrient addition) on pollinator-mediated selection on floral traits of Primula tibetica (an insect-pollinated perennial herbaceous species). Our results demonstrated that floral traits, plant reproductive success and pollinator-mediated selection on floral traits varied between sites with different soil water contents and among different levels of nutrient addition. The strength of pollinator-mediated selection was stronger at the site with low soil water content than at the site with high soil water content, and first decreased and then increased with increasing N-P-K nutrient addition. Our results support the hypothesis that abiotic environmental factors influence the importance of pollinators in shaping floral evolution.

The evolution of floral traits in animal-pollinated plants involves the interaction between flowers as signal senders and pollinators as signal receivers. Flower colors are very diverse, effect pollinator attraction and flower foraging behavior, and are hypothesized to be shaped through pollinator-mediated selection. However, most of our current understanding of flower color evolution arises from variation between discrete color morphs and completed color shifts accompanying pollinator shifts, while evidence for pollinator-mediated selection on continuous variation in flower colors within populations is still scarce. In this review, we summarize experiments quantifying selection on continuous flower color variation in natural plant populations in the context of pollinator interactions. We found that evidence for significant pollinator-mediated selection is surprisingly limited among existing studies. We propose several possible explanations related to the complexity in the interaction between the colors of flowers and the sensory and cognitive abilities of pollinators as well as pollinator behavioral responses, on the one hand, and the distribution of variation in color phenotypes and fitness, on the other hand. We emphasize currently persisting weaknesses in experimental procedures, and provide some suggestions for how to improve methodology. In conclusion, we encourage future research to bring together plant and animal scientists to jointly forward our understanding of the mechanisms and circumstances of pollinator-mediated selection on flower color.

Visual and olfactory floral signals play key roles in plant-pollinator interactions. In recent decades, studies investigating the evolution of either of these signals have increased considerably. However, there are large gaps in our understanding of whether or not these two cue modalities evolve in a concerted manner. Here, we characterized the visual (i.e., color) and olfactory (scent) floral cues in bee-pollinated Campanula species by spectrophotometric and chemical methods, respectively, with the aim of tracing their evolutionary paths. We found a species-specific pattern in color reflectance and scent chemistry. Multivariate phylogenetic statistics revealed no influence of phylogeny on floral color and scent bouquet. However, univariate phylogenetic statistics revealed a phylogenetic signal in some of the constituents of the scent bouquet. Our results suggest unequal evolutionary pathways of visual and olfactory floral cues in the genus Campanula. While the lack of phylogenetic signal on both color and scent bouquet points to external agents (e.g., pollinators, herbivores) as evolutionary drivers, the presence of phylogenetic signal in at least some floral scent constituents point to an influence of phylogeny on trait evolution. We discuss why external agents and phylogeny differently shape the evolutionary paths in floral color and scent of closely related angiosperms.

Indirect species interactions are ubiquitous in nature, often outnumbering direct species interactions. Yet despite evidence that indirect interactions have strong ecological effects, relatively little is known about whether they can shape adaptive evolution by altering the strength and/or direction of natural selection. We tested whether indirect interactions affect the strength and direction of pollinator-mediated selection on floral traits of the bumble-bee pollinated wildflower Lobelia siphilitica. We estimated the indirect effects of two pollinator predators with contrasting hunting modes: dragonflies (Aeshnidae and Corduliidae) and ambush bugs (Phymata americana, Reduviidae). Because dragonflies are active pursuit predators, we hypothesized that they would strengthen pollinator-mediated selection by weakening plant-pollinator interactions (i.e., a density-mediated indirect effect). In contrast, because ambush bugs are sit-and-wait predators, we hypothesized that they would weaken or reverse the direction of pollinator-mediated selection by altering pollinator foraging behavior (i.e., a trait-mediated indirect effect). Specifically, if ambush bugs hunt from plants with traits that attract pollinators (i.e., prey), then pollinators will spend less time visiting those plants, weakening or reversing the direction of selection on attractive floral traits. We did not find evidence that high dragonfly abundance strengthened selection on floral traits via a density-mediated indirect effect: neither pollen limitation (a proxy for the strength of plant-pollinator interactions) nor directional selection on floral traits of L. siphilitica differed significantly between high- and low-dragonfly abundance treatments. In contrast, we did find evidence that ambush bug presence affected selection on floral traits via a trait-mediated indirect effect: ambush bugs hunted from L. siphilitica plants with larger daily floral displays, reversing the direction of pollinator-mediated selection on daily display size. These results suggest that indirect species interactions have the potential to shape adaptive evolution by altering natural selection.

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.