On the ecological significance of pollen color: a case study in American trout lily (Erythronium americanum).

Evolutionary ecologists seek to explain the processes that maintain variation within populations. In plants, petal color variation can affect pollinator visitation, environmental tolerance, and herbivore deterrence. Variation in sexual organs may similarly affect plant performance. Within-population variation in pollen color, as occurs in the eastern North American spring ephemeral Erythronium americanum, provides an excellent opportunity to investigate the maintenance of variation in this trait. Although the red/yellow pollen-color polymorphism of E. americanum is widely recognized, it has been poorly documented. Our goals were thus (1) to determine the geographic distribution of the color morphs and (2) to test the effects of pollen color on components of pollen performance. Data provided by citizen scientists indicated that populations range from monomorphic red, to polymorphic, to monomorphic yellow, but there was no detectable geographic pattern in morph distribution, suggesting morph occurrence cannot be explained by a broad-scale ecological cline. In field experiments, we found no effect of pollen color on the probability of predation by the pollen-feeding beetle Asclera ruficollis, on the ability of pollen to tolerate UV-B radiation, or on siring success (as measured by the fruit set of hand-pollinated flowers). Pollinators, however, exhibited site-specific pollen-color preferences, suggesting they may act as agents of selection on this trait, and, depending on the constancy of their preferences, could contribute to the maintenance of variation. Collectively, our results eliminate some hypothesized ecological effects of pollen color in E. americanum, and identify effects of pollen color on pollinator attraction as a promising direction for future investigation.

Explaining the apparent paradox of persistent selection for early flowering.

Decades of observation in natural plant populations have revealed pervasive phenotypic selection for early flowering onset. This consistent pattern seems at odds with life-history theory, which predicts stabilizing selection on age and size at reproduction. Why is selection for later flowering rare? Moreover, extensive evidence demonstrates that flowering time can and does evolve. What maintains ongoing directional selection for early flowering? Several non-mutually exclusive processes can help to reconcile the apparent paradox of selection for early flowering. We outline four: selection through other fitness components may counter observed fecundity selection for early flowering; asymmetry in the flowering-time-fitness function may make selection for later flowering hard to detect; flowering time and fitness may be condition-dependent; and selection on flowering duration is largely unaccounted for. In this Viewpoint, we develop these four mechanisms, and highlight areas where further study will improve our understanding of flowering-time evolution.

Estimating selection through male fitness: three complementary methods illuminate the nature and causes of selection on flowering time.

Our understanding of selection through male fitness is limited by the resource demands and indirect nature of the best available genetic techniques. Applying complementary, independent approaches to this problem can help clarify evolution through male function. We applied three methods to estimate selection on flowering time through male fitness in experimental populations of the annual plant Brassica rapa: (i) an analysis of mating opportunity based on flower production schedules, (ii) genetic paternity analysis, and (iii) a novel approach based on principles of experimental evolution. Selection differentials estimated by the first method disagreed with those estimated by the other two, indicating that mating opportunity was not the principal driver of selection on flowering time. The genetic and experimental evolution methods exhibited striking agreement overall, but a slight discrepancy between the two suggested that negative environmental covariance between age at flowering and male fitness may have contributed to phenotypic selection. Together, the three methods enriched our understanding of selection on flowering time, from mating opportunity to phenotypic selection to evolutionary response. The novel experimental evolution method may provide a means of examining selection through male fitness when genetic paternity analysis is not possible.

Temporal variation in phenotypic gender and expected functional gender within and among individuals in an annual plant.

BACKGROUND AND AIMS: Adaptive explanations for variation in sex allocation centre on variation in resource status and variation in the mating environment. The latter can occur when dichogamy causes siring opportunity to vary across the flowering season. In this study, it is hypothesized that the widespread tendency towards declining fruit-set from first to last flowers on plants can similarly lead to a varying mating environment by causing a temporal shift in the quality (not quantity) of siring opportunities. METHODS: A numerical model was developed to examine the effects of declining fruit-set on the expected male versus female reproductive success (functional gender) of first and last flowers on plants, and of early- and late-flowering plants. Within- and among-plant temporal variation in pollen production, ovule production and fruit-set in 70 Brassica rapa plants was then characterized to determine if trends in male and female investment mirror expected trends in functional gender. KEY RESULTS: Under a wide range of model conditions, functional femaleness decreased sharply in the last flowers on plants, and increased from early- to late-flowering plants in the population. In B. rapa, pollen production decreased more rapidly than ovule production from first to last flowers, leading to a within-plant increase in phenotypic femaleness. Among plants, ovule production decreased from early- to late-flowering plants, causing a temporal decrease in phenotypic femaleness. CONCLUSIONS: The numerical model confirmed that declining fruit-set can drive temporal variation in functional gender, especially among plants. The discrepancy between observed trends in phenotypic gender in B. rapa and expected functional gender predicted by the numerical model does not rule out the possibility that male reproductive success decreases with later flowering onset. If so, plants may experience selection for early flowering through male fitness.

Global urban environmental change drives adaptation in white clover.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Photoinactivation of Photosystem II in Prochlorococcus and Synechococcus.

The marine picocyanobacteria Synechococcus and Prochlorococcus numerically dominate open ocean phytoplankton. Although evolutionarily related they are ecologically distinct, with different strategies to harvest, manage and exploit light. We grew representative strains of Synechococcus and Prochlorococcus and tracked their susceptibility to photoinactivation of Photosystem II under a range of light levels. As expected blue light provoked more rapid photoinactivation than did an equivalent level of red light. The previous growth light level altered the susceptibility of Synechococcus, but not Prochlorococcus, to this photoinactivation. We resolved a simple linear pattern when we expressed the yield of photoinactivation on the basis of photons delivered to Photosystem II photochemistry, plotted versus excitation pressure upon Photosystem II, the balance between excitation and downstream metabolism. A high excitation pressure increases the generation of reactive oxygen species, and thus increases the yield of photoinactivation of Photosystem II. Blue photons, however, retained a higher baseline photoinactivation across a wide range of excitation pressures. Our experiments thus uncovered the relative influences of the direct photoinactivation of Photosystem II by blue photons which dominates under low to moderate blue light, and photoinactivation as a side effect of reactive oxygen species which dominates under higher excitation pressure. Synechococcus enjoyed a positive metabolic return upon the repair or the synthesis of a Photosystem II, across the range of light levels we tested. In contrast Prochlorococcus only enjoyed a positive return upon synthesis of a Photosystem II up to 400 µmol photons m-2 s-1. These differential cost-benefits probably underlie the distinct photoacclimation strategies of the species.

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.

What drives selection on flowering time? An experimental manipulation of the inherent correlation between genotype and environment.

The optimal timing of the seasonal switch from somatic growth to reproduction can depend on an individual's condition at reproduction, the quality of the environment in which it will reproduce, or both. In annual plants, vegetative size (a function of age at flowering) affects resources available for seed production, whereas exposure to mutualists, antagonists, and abiotic stresses in the environment (functions of Julian date of flowering) influences success in converting resources into offspring. The inherent tight correlation between age, size, and environment obscures their independent fitness contributions. We isolated the fitness effects of these factors by experimentally manipulating the correlation between age at flowering and date of flowering in Brassica rapa. We staggered the planting dates of families with differing ages at flowering to produce experimental populations in which age at flowering and date of flowering were positively, negatively, or uncorrelated. In all populations, plants with an early date of flowering produced more seed than those flowering late, regardless of age or size at flowering onset. The temporal environment was thus the principal driver of selection on flowering time, but its importance relative to that of age and size varied with the presence/absence of herbivores and seed predators.

Hard and soft selection on phenology through seasonal shifts in the general and social environments: A study on plant emergence time.

The timing of transition out of one life-history phase determines where in the seasonal succession of environments the next phase is spent. Shifts in the general environment (e.g., seasonal climate) affect the expected fitness for particular transition dates. Variation in transition date also leads to temporal variation in the social environment. For instance, early transition may confer a competitive advantage over later individuals. If so, the social environment will impose frequency- and density-dependent selection components. In effect, the general environment imposes hard selection, whereas the social environment imposes soft selection on phenology. We examined hard and soft selection on seedling emergence time in an experiment on Brassica rapa. In monoculture (uniform social environment), early emergence results in up to a 1.5-fold increase in seed production. In bicultures (heterogeneous social environment), early-emerging plants capitalized on their head start, suppressing their late neighbors and increasing their fitness advantage to as much as 38-fold, depending on density. We devised a novel adaptation of contextual analysis to partition total selection (i.e., cov(ω, z)) into the hard and soft components. Hard and soft components had similar strengths at low density, whereas soft selection was five times stronger than hard at high density.