Stable two-allele polymorphisms maintained by fluctuating fitnesses and seed banks: protecting the blues in Linanthus parryae

Motivated by data demonstrating fluctuating relative and absolute fitnesses for white- versus blue-flowered morphs of the desert annual Linanthus parryae, we present conditions under which temporally fluctuating selection and fluctuating contributions to a persistent seed bank will maintain a stable single-locus polymorphism. In L. parryae, blue flower color is determined by a single dominant allele. To disentangle the underlying diversity-maintaining mechanism from the mathematical complications associated with departures from Hardy-Weinberg genotype frequencies and dominance, we successively analyze a haploid model, a diploid model with three distinguishable genotypes, and a diploid model with complete dominance. For each model, we present conditions for the maintenance of a stable polymorphism, then use a diffusion approximation to describe the long-term fluctuations associated with these polymorphisms. Our protected polymorphism analyses show that a genotype whose arithmetic and geometric mean relative fitnesses are both less than one can persist if its relative fitness exceeds one in years that produce the most offspring. This condition is met by data from a population of L. parryae whose white morph has higher fitness (seed set) only in years of relatively heavy rain fall. The data suggest that the observed polymorphism may be explained by fluctuating selection. However, the yearly variation in flower color frequencies cannot be fully explained by our simple models, which ignore age structure and possible selection in the seed bank. We address two additional questions--one mathematical, the other biological--concerning the applicability of diffusion approximations to intense selection and the applicability of long-term predictions to datasets spanning decades for populations with long-lived seed banks.     

Pollinator response to flower color polymorphism and floral display in a plant with a single-locus floral color polymorphism: consequences for plant reproduction

Variation in flower color, particularly polymorphism, in which two or more different flower color phenotypes occur in the same population or species, may be affected or maintained by mechanisms that depend on pollinators. Furthermore, variation in floral display may affect pollinator response and plant reproductive success through changes in pollinator visitation and availability of compatible pollen. To asses if flower color polymorphism and floral display influences pollinator preferences and movements within and among plants and fitness-related variables we used the self-incompatible species Cosmos bipinnatus Cav. (Asteraceae), a model system with single-locus flower color polymorphism that comprises three morphs: white (recessive homozygous), pink (heterozygous co-dominate), and purple (dominant homozygous) flowers. We measured the preferences of pollinators for each morph and constancy index for each pollinator species, pollination visitation rate, floral traits, and female fitness measures. Flower color morphs differed in floral trait measures and seed production. Pollinators foraged nonrandomly with respect to flower color. The most frequent morph, the pink morph, was the most visited and pollinators exhibited the highest constancy for this morph. Moreover, this morph exhibited the highest female fitness. Pollinators responded strongly to floral display size, while probed more capitulums from plants with large total display sizes, they left a great proportion of them unvisited. Furthermore, total pollinator visitation showed a positive relation with female fitness. Results suggest that although pollinators preferred the heterozygous morph, they alternate indiscriminately among morphs making this polymorphism stable.     

Inheritance of flower color in pickerelweed (Pontederia cordata L.)

Pickerelweed (Pontederia cordata L.) is a diploid (2n = 2x = 16), erect, emergent, herbaceous aquatic perennial. The showy inflorescences of pickerelweed make this species a prime candidate for inclusion in water gardens and aquascapes. The objective of this experiment was to determine the number of loci, number of alleles, and gene action controlling flower color (blue vs. white) in pickerelweed. Two blue-flowered and one white-flowered parental lines were used in this experiment to create S(1) and F(1) populations. F(2) populations were produced through self-pollination of F(1) plants. Evaluation of S(1), F(1), and F(2) generations revealed that flower color in these populations was controlled by 2 alleles at one locus with blue flower color completely dominant to white. We propose that this locus be named white flower with alleles W and w.     

Linking frugivores to the dynamics of a fruit color polymorphism

Although fruit color polymorphisms are a widespread phenomenon, the role of frugivores in their maintenance is unknown. Selection would require that frugivores interact differentially with fruit color morphs to alter their relative fitnesses, but such a pattern has yet to be demonstrated. In a 3-yr field study, the interactions of ants and birds with Acacia ligulata, an Australian shrub with a red/yellow/ orange aril color polymorphism, were examined. Bird species fell into three feeding guilds: seed dispersers, seed predators, and aril thieves; ant species acted either as seed dispersers or aril thieves. While there was no evidence of morph bias in ants, in some years birds fed more frequently on the yellow and orange morphs. Based on patterns of seedling survival and juvenile recruitment in seed deposition sites, bird seed dispersers increased the fitness of yellow and orange morphs (relative to red) in some populations, but decreased their relative fitness in others. Bird seed predators uniformly reduced relative fitness of yellow and orange morphs, while bird aril thieves had unknown effects. Altogether, consumer biases produced spatiotemporal variability in the relative fitness of A. ligulata color morphs, a pattern qualitatively consistent with maintenance of the polymorphism.     

THE IMPACT OF A FLOWER-COLOR POLYMORPHISM ON MATING PATTERNS IN EXPERIMENTAL POPULATIONS OF WILD RADISH (RAPHANUS RAPHANISTRUM L.)

We conducted field experiments to determine how a naturally occurring petal-color polymorphism influences mating patterns in wild radish (Raphanus raphanistrum). The polymorphism is controlled at a single genetic locus, with white petal color being completely dominant to yellow. In experimental populations with equal numbers of yellow- and white-flowered homozygous individuals, insect visitors strongly discriminated against white flowers. Pieris rapae, the most frequent pollinator, was almost 50% more likely to visit yellow than white flowers. Maternal fecundity did not differ between the morphs and was not significantly influenced by a plant's compatibility with potential donors, suggesting that seed production was not limited by receipt of compatible pollen. In contrast, the yellow-flowered morph sired approximately 75% of all seeds produced during the study. This paternity proportion was consistently greater than that expected on the basis of postpollination compatibility measures and was indistinguishable from that expected on the basis of pollinator-visitation frequency. We conclude that the male-fitness advantage of the yellow morph resulted from enhanced pollen export due to the greater attractiveness of its flowers to insect pollinators. With color morphs evenly distributed in experimental arrays, insects did not move assortatively on the basis of petal color, and we found no evidence for assortative pollen flow due to the floral polymorphism. Once postpollination compatibility relationships within populations were taken into account, paternal success of yellow donors did not differ between yellow- and white-flowered maternal plants.     

POLLINATION AND SEED PRODUCTION IN IPOMOPSIS AGGREGATA: DIFFERENCES AMONG AND WITHIN FLOWER COLOR MORPHS

The pollination of red, pink, and white color morphs of Ipomopsis aggregata was evaluated to assess whether ethological isolation based on pollinator color discrimination may occur. We observed animal visitors, assessed pollen delivery, seed set per fruit, percentage of flowers setting fruit, nectar production, and timing of flower opening for different color morphs in the Front Range of Colorado. Based on traditional zoophilous flower classifications, we expected hummingbirds to pollinate red-flowered I. aggregata subsp. collina and hawkmoths to pollinate white-flowered I. aggregata subsp. Candida. However, ethological isolation does not appear to occur among color morphs of I. aggregata in the Front Range. Hummingbirds visited red-flowered plants in excess overall, and, to a lesser extent, so did hawkmoths. Both hummingbirds and hawkmoths visited all color morphs and probably transferred pollen among them. Pollen delivery data and a day-night bagging experiment also suggest that pollinators do not necessarily behave as predicted by flower classifications. In addition, there is little evidence for major differences between red, white, and pink flowers in any aspects of reproductive biology. Indeed, most variation occurs within a given color morph.     

Discovery of gynoecium color polymorphism in an aquatic plant

Flower color polymorphlsm exhibited by natural populations provides an opportunity for understanding the evolutionary mechanisms contributing to the diversity of floral morphology.However,little is known about the color polymorphism of female organs in flowering plants.Here we report gynoecium color polymorphism in Butomus umbellatus (Butomaceae),an emergent,aquatic monocot.Populations from Mishan,northeastern China comprised two morphs; gynoecia are either pink,as observed in other areas,or white.We measured floral traits and female fecundity in the two gynoecium color morphs in the field.There was no significant difference in plant height,pedicel length,and flower size including petal,sepal and gynoecium between the two morphs,but plants with pink gynoecia had wider inflorescence stalks,larger inner whorl anthers and produced more pollen and ovules than those with white gynoecia.Correspondingly,we found that seed production was significantly higher in the pink than in the white morph.This new finding suggested selection against white gynoecia in part because of low fecundity,consistent with the rarity of the white gynoecium morph in this species.     

Pollen colour morphs take different paths to fitness

Colour phenotypes are often involved in communication and are thus under selection by species interactions. However, selection may also act on colour through correlated traits or alternative functions of biochemical pigments. Such forms of selection are instrumental in maintaining petal colour diversity in plants. Pollen colour also varies markedly, but the maintenance of this variation is little understood. In Campanula americana, pollen ranges from white to dark purple, with darker morphs garnering more pollinator visits and exhibiting elevated pollen performance under heat stress. Here, we generate an F2 population segregating for pollen colour and measure correlations with floral traits, pollen attributes and plant‐level traits related to fitness. We determine the pigment biochemistry of colour variants and evaluate maternal and paternal fitness of light and dark morphs by crossing within and between morphs. Pollen colour was largely uncorrelated with floral traits (petal colour, size, nectar traits) suggesting it can evolve independently. Darker pollen grains were larger and had higher anthocyanin content (cyanidin and peonidin) which may explain why they outperform light pollen under heat stress. Overall, pollen‐related fitness metrics were greater for dark pollen, and dark pollen sires generated seeds with higher germination potential. Conversely, light pollen plants produce 61% more flowers than dark, and 18% more seeds per fruit, suggesting a seed production advantage. Results indicate that light and dark morphs may achieve fitness through different means—dark morphs appear to have a pollen advantage whereas light morphs have an ovule advantage—helping to explain the maintenance of pollen colour variation.     

Direct and indirect selection on floral pigmentation by pollinators and seed predators in a color polymorphic South African shrub

The coexistence of different color morphs is often attributed to variable selection pressures across space, time, morph frequencies, or selection agents, but the routes by which each morph is favored are rarely identified. In this study we investigated factors that influence floral color polymorphisms on a local scale in Protea, within which approximately 40% of species are polymorphic. Previous work shows that seed predators and reproductive differences likely contribute to maintaining polymorphism in four Protea species. We explored whether selection acts directly or indirectly on floral color in two populations of Protea aurea, using path analysis of pollinator behavior, nectar production, seed predation, color, morphology, and maternal fecundity fitness components. We found that avian pollinators spent more time on white morphs, likely due to nectar differences, but that this had no apparent consequences for fecundity. Instead, the number of flowers per inflorescence underpinned many of the reproductively important differences between color morphs. White morphs had more flowers per inflorescence, which itself was positively correlated with nectar production, seed predator occurrence, and total long-term seed production. The number of seeds per plant to survive predation, in contrast, was not directly associated with color or any other floral trait. Thus, although color differences may be associated with conflicting selection pressures, the selection appears to be associated with the number of flowers per inflorescence and its unmeasured correlates, rather than with inflorescence color itself.     

MEASUREMENTS OF NATURAL SELECTION ON FLORAL TRAITS IN WILD RADISH (RAPHANUS RAPHANISTRUM). I. SELECTION THROUGH LIFETIME FEMALE FITNESS

Although the role of natural selection in the evolution of floral traits has been of great interest to biologists since Darwin, studies of selection on floral traits through differences in lifetime fitness have been rare. We measured selection acting on flower number, flower size, stigma exsertion, and ovule number per flower using field data on lifetime female fitness (seed production) in wild radish, Raphanus raphanistrum. The patterns of selection were reasonably consistent across three field seasons, with strong directional selection for increased flower production in all three years, weaker selection for increased ovule number per flower in two years, and selection for increased flower size in one year. The causes of the selection were investigated using path analysis combined with multiplicative fitness components. Increased flower production increased fruit production directly, and increased numbers of ovules per flower increased the number of seeds per fruit in all three years; pollinator visitation did not influence either of these fitness components. Increased flower size was associated with increases in both the number of fruit and the number of seeds per fruit in one year, with the latter relationship being stronger. Total lifetime seed production was affected more strongly by differences in fruit production than by differences in either the number of seeds per fruit or the proportion of fertilized seeds that were viable, but all three fitness components were positively correlated with total seed production.     

SPATIAL DIFFERENTIATION FOR FLOWER COLOR IN THE DESERT ANNUAL LINANTHUS PARRYAE: WAS WRIGHT RIGHT?

Understanding the evolutionary mechanisms that contribute to the local genetic differentiation of populations is a major goal of evolutionary biology, and debate continues regarding the relative importance of natural selection and random genetic drift to population differentiation. The desert plant Linanthus parryae has played a prominent role in these debates, with nearly six decades of empirical and theoretical work into the causes of spatial differentiation for flower color. Plants produce either blue or white flowers, and local populations often differ greatly in the frequencies of the two color morphs. Sewall Wright first applied his model of "isolation by distance" to investigate spatial patterns of flower color in Linanthus. He concluded that the distribution of flower color morphs was due to random genetic drift, and that Linanthus provided an example of his shifting balance theory of evolution. Our results from comprehensive field studies do not support this view. We studied an area in which flower color changed abruptly from all-blue to all-white across a shallow ravine. Allozyme markers sampled across these regions showed no evidence of spatial differentiation, reciprocal transplant experiments revealed natural selection favoring the resident morph, and soils and the dominant members of the plant community differed between regions. These results support the hypothesis that local differences in flower color are due to natural selection, not due to genetic drift.     

Effects of local density and flower colour polymorphism on pollination and reproduction in the rewardless orchid Dactylorhiza sambucina (L.) Soò

The rewardless orchid Dactylorhiza sambucina shows a stable flower colour polymorphism, with both yellow- and red-flowered morphs growing sympatrically. Pollination biology and breeding system were investigated to examine the effects of density of plants, colour polymorphism, inflorescence dimension, and flower position within inflorescence on male and female reproductive success in three natural populations of D. sambucina. There were significant differences among sites in the number of pollinia removed and in fruit set per inflorescence. Number of removed pollinia and capsule production in D. sambucina were independent from flower and inflorescence size or flower position. As a whole, the red morphs showed the highest number of capsules produced, while the yellow morphs had the greatest male success. The relative male and female reproductive success were independent from plant density but were significantly correlated with the yellow morph frequency at the population level. Overall, our findings show that the contribution to the total reproductive success deriving from the two colour morphs does not conform with the predictions of negative frequency-dependent selection.     

Inheritance of flower color in chickpea

Flower color is a useful morphological marker in chickpea (Cicer arietinum L.). Inheritance of this trait was studied using two white-flowered chickpea genotypes, P 9623 and RS 11, and one blue-flowered genotype, T 39-1. The genetic constitutions of the white flower colors of P 9623 and RS 11 were different, for in an earlier study their F1 produced pink flowers. The two F1s of the crosses P 9623 x T 39-1 and RS 11 x T 39-1 also produced pink flowers. Each of the two F2 populations segregated in 9 pink:3 blue:4 white-flowered plants. These results can be explained by a three-gene model. These three independently segregating genes are probably the same as C, B, and P reported in the literature earlier. Allelic tests could not be undertaken, as the genetic stocks used in the earlier studies are not available. The genetic constitutions of the three parents and their F1s are proposed. These accessions should be useful for conducting allelic tests for determining flower color loci in chickpea and for comparative studies with field pea. The seeds of these genetic stocks are maintained at the Genetic Resources and Enhancement Program at ICRISAT and are available for research purposes on request.     

FERTILITY SELECTION ON A DISCRETE FLORAL POLYMORPHISM IN CLARKIA (ONAGRACEAE)

This study investigated fertility selection on a flower petal pigmentation polymorphism in Clarkia gracilis ssp. sonomensis. Natural populations are typically composed of nearly 100% spotted-petal plants, although rare populations contain a majority of unspotted plants. I compared fitness values for the two morphs using a simple fertility model to estimate selection for experimental arrays of plants placed into existing populations of different phenotypic frequencies. Both male and female reproductive success were estimated as well as the pattern of mating among phenotypes. Although the separate fitness components varied from no differences to a strong advantage for spotted plants, for every situation the selection calculations predicted an increase in the frequency of the spotted allele. Pollinator behavior and postpollination mechanisms may be responsible for the fitness differences. The apparent inability of the unspotted allele to spread though most natural populations is consistent with its selective disadvantage in this study.     

Sex allocation of females and hermaphrodites in the gynodioecious Geranium sylvaticum

Seed production and patterns of sex allocation were studied in female and hermaphroditic plants in two gynodioecious populations of Geranium sylvaticum (Geraniaceae). Females produced more flower buds and seeds than hermaphrodites in one of the two study populations. The other female traits measured (pistil biomass, seed number per fruit, individual seed mass) did not differ between the gender morphs. The relative seed fitness of hermaphrodites differed between the study populations, with hermaphrodites gaining less of their fitness through female function in the population with a high frequency of females. However, the amount and size of pollen produced by hermaphrodites did not differ between populations. The number of flower buds was positively correlated with seed production in females, whereas in hermaphrodites a positive correlation between number of buds and seed production was found in only one of the two study populations. These results suggest that fitness gain through female function is labile in hermaphrodites of this species, and is probably affected by environmental factors such as the sex ratio of the population.     

Floral Color Polymorphism and Reproductive Success in Annatto (Bixa orellana L.)

Floral color polymorphism of annatto (Bixa orellana L.) offers a wide range of colors that are maintained in the population by either pollinators or non pollinator agents of selection. In the present study, maintenance of different floral colors was analyzed in relation to reproductive success of Bixa orellana. The different floral petal colors (white, amaranth rose, petunia purple or cobalt violet) were determined from selected plants with reflectance spectrophotometry. Phenotypic measures of other floral traits, female reproductive success, seed set, seed output and seed weight also revealed variation between different floral morphs. Records on seed set varied significantly for different floral color morphs. Maximum fruit maturation (58 %) was observed in amaranth rose and least fruit maturation (25 %) in the white morph. Seed set data indicates pollinators’ preference for more intensely colored flowers. This preference may be due to ability of the pollinators to distinguish the morphs through differentially reduced sensitivity at the green wavelengths. In flowers which received fewer insect visits, polymorphism might be maintained by self fertilization. The color morphs showed differences in Random Amplified Polymorphic DNA (RAPD) profile indicating a genetic basis for floral color variation and consequent differences in seed set. Out of 88 bands generated with nine operon primers, 70 were polymorphic. The present study provides valuable information on the influence of petal color on maternal fitness in B. orellana.     

Multiple herbivores and coevolutionary interactions in an Ipomopsis hybrid swarm

Studies focusing on pairwise interactions between plants and herbivores may not give an accurate picture of the overall selective effect of herbivory, given that plants are often eaten by a diverse array of herbivore species. The outcome of such interactions may be further complicated by the effects of plant hybridization. Hybridization can lead to changes in morphological, phenological and chemical traits that could in turn alter plant–herbivore interactions. Here we present results from manipulative field experiments investigating the interactive effects of multiple herbivores and plant hybridization on the reproductive success of Ipomopsis aggregata formosissima X I. tenuituba. Results showed that ungulate herbivores alone had a net positive effect on plant relative fitness, increasing seed production approximately 2-fold. Caterpillars had no effect on plant relative fitness when acting alone, with caterpillar-attacked plants producing the same number of flowers, fruits and seeds as the uneaten controls. Caterpillars, however, significantly reduced flower production of ungulate browsed plants. Flower production in these plants, however, was still significantly greater (approximately 1.7-fold greater) than uneaten controls, likely leading to an increase in reproductive success through the paternal component of fitness given that fruit and seed production was not significantly different from that of herbivore-free controls. Although results suggest that herbivore imposed selection is pairwise, ungulates likely have a large influence on the abundance of, and hence the amount of damage caused by, caterpillar herbivores. Thus, because of the ecological interactions between ungulates and caterpillars, selection on Ipomopsis may be diffuse rather than pairwise, assuming such interactions translate into differential effects on plant fitness as herbivore densities vary. Plant hybridization had no significant effect on patterns of ungulate or caterpillar herbivory; i.e., no significant interactions were detected between herbivory and plant hybridization for any of the fitness traits measured in this study nor did plant hybridization have any significant effect on host preference. These results may be due to patterns of introgression or the lack of species-specific differences between I. aggregate formosissima and I. tenuituba. Plant hybridization per se resulted in lowered reproductive success of white colored morphs due in part to the effects of pollination. Although it appears that there would be strong directional selection favoring darker flower colors due to the lower reproductive success of the white colored morphs in the short run, the natural distribution of hybrids suggest that over the long run selection either tends to average out or there are no fitness differences among morphs in most years due to the additive fitness effects of hawkmoth and hummingbird pollinators.     

Dry environments promote the establishment of females in monomorphic populations of <Emphasis Type="Italic">Wurmbea biglandulosa</Emphasis> (Colchicaceae)

In flowering plants, the evolution of dimorphic breeding systems from monomorphic ancestors can be associated with dry environments. One hypothesis to explain this pattern is that seed fertility of hermaphrodites decreases more than seed fertility of females under dry conditions, so that females have greater relative fitness. This could occur if seed production of hermaphrodites is more resource-limited than that of females, or shifts in pollination increase levels of selfing and inbreeding depression in hermaphrodites. Here we assess the role of dry environments in promoting a female fitness advantage in Wurmbea biglandulosa by focusing on monomorphic and dimorphic populations that occur along a longitudinal gradient of decreasing rainfall. Dimorphic populations occurred in sites with higher temperatures, lower rainfall and lower soil moisture. Overall, females had greater seed fertility than did hermaphrodites from monomorphic populations, which in turn had greater seed fertility than hermaphrodites from dimorphic populations. Ovuliferous flower and ovule production by the three gender morphs and seed fertility of females and hermaphrodites in monomorphic populations did not vary with soil moisture. By contrast, seed fertility of hermaphrodites in dimorphic populations was positively related to soil moisture. Accordingly, female frequency was higher in those sites where hermaphrodites produced relatively fewer seeds. Taken together our results indicate that dry environments promote the establishment of females by decreasing the relative seed fitness of hermaphrodites. Moreover, because seed fertility of hermaphrodites in monomorphic populations did not vary with soil moisture, resource limitation of female function may play only a minor role in the establishment of females. Other factors such as shifts in pollination and mating patterns of hermaphrodites could be involved. Key words:breeding system evolution, environmental stress, gender dimorphism, gynodioecy, sex ratio variationCo-ordinating editor: J.F. Stuefer     

Solitary plants do as well as clumped ones in Silene uniflora (Caryophyllaceae)

Many studies have been done on seed production as a function of population density in wild plants Most of them show a higher seed-set per flower of densely growing plants In this study, in a gynodioecious Silene uniflora (Caryophyllaceae) population on the Baltic island of Oland, high plant density did not increase fruit-set or seed-set Instead, the total number of seeds set was slightly higher for widely scattered plants as a result of a somewhat lower number of ovules per flower in densely growing plants Individuals had nothing to gain by growing close together, because there was no reproductive parameter which could compensate for the low ovule number per flower of closely growing plants Plant size determined the total seed production of individuals, but did not correlate with any of the fitness components studied per flower basis The different gender morphs showed the same pattern, which is discussed as a comparison with pollen limitation in self-incompatible and self-incompatible plants     

The effect of nectar guides on pollinator preference: experimental studies with a montane herb

Summary Rare albino morphs of the montane larkspur Delphinium nelsonii differ from common blue-flowered morphs in overall flower color, and in the strength of a contrasting color pattern at the center of the flower that presumably guides pollinators to concealed nectar. Previous studies showed that bumblebees and hummingbirds discriminate against albinos when presented with mixtures of the 2 morphs, and that it takes these pollinators longer to fly between successive flowers on albino than on blue-flowered inflorescences. To explore the link between these observations, we measured pollinator preferences and flower-to-flower flight times (handling times) before and after painting flowers in 2 alternative ways that enhanced albino nectar guides. In all of 16 experimental replicates discrimination against albinos was reduced or eliminated after painting, and albino handling times declined toward values for blue-flowered inflorescences. This consistent result indicates that an inferior nectar guide increases the energetic cost of foraging at albinos. Increased cost in turn explains discrimination, under the reasonable assumption that hummingbirds and bumblebees are sensitive to foraging economics.