Floral color variation and associations with fitness‐related traits in Malva moschata (Malvaceae)

Genetic polymorphisms for floral color are interesting phenomena to study because they are likely to be maintained by opposing selective forces. Pollinator preferences may exert direct selection on floral color; however, floral color might also be the indirect target of selection through genetic associations with other traits under selection. Malva moschata (Malvaceae) is a North American species that produces either red or white flowers. In the present study, we present reflectance spectrophotometry data that characterize the nature of floral color variation in this species and show that honey bees and bumble bees should be able to distinguish between the morphs through differential sensitivity at the green (long‐wavelength) photoreceptor. Second, we use a series of phenotypic measures to investigate whether the color morphs differ with respect to other floral traits, vegetative traits or female reproductive success, and use a series of correlation analyses to infer the relative independence of color from these other traits. We found that red‐flowered morphs produced more anthers per flower and had greater leaf area, and that white‐flowered morphs had greater percentage fruit set; however, there were no reproductive success differences between the morphs. The relationship between flower size and anther number was the only correlation that differed between the morphs. Finally, a series of pollinator‐choice experiments showed that bumble bees strongly prefer red morphs in terms of visit frequency and duration, but honey bees have no preference. Taken together, our results suggest that color is rather independent of other phenotypic traits, and that honey bee abundance is likely to play a role in maintaining color variation in this system.     

Opposing natural selection from herbivores and pathogens may maintain floral-color variation in Claytonia virginica (Portulacaceae)

The maintenance of floral-color variation within natural populations is enigmatic because directional selection through pollinator preferences combined with random genetic drift should lead to the rapid loss of such variation. Fluctuating, balancing, and negative frequency-dependent selection mediated through pollinators have been identified as factors that may contribute to the maintenance of floral-color variation, and recently it has been suggested that indirect responses to selection on correlated characters through agents of selection other than pollinators may substantially shape the evolution of floral traits. Here, I provide empirical support for this latter view in Claytonia virginica (Portulacaceae) through a multiseason field study, a pollen supplementation study, and an artificial herbivory experiment. These studies show that most individuals fall into one of four discrete color classes, and suggest pollinator-mediated selection for increased floral redness in concurrent years. Floral color is also an indirect target of opposing directional selection via herbivores and pathogens that fluctuates through time. Taken together, these data suggest a novel mechanism by which floral-color variation may be maintained, and illustrate the importance of an inclusive, pluralistic view of selection when investigating the evolution of complex phenotypes.     

The adaptive value of phenotypic floral integration

Floral integration has been deemed an adaptation to increase the benefits of animal pollination, yet no attempts have been made to estimate its adaptive value under natural conditions. Here, the variation in the magnitude and pattern of phenotypic floral integration and the variance-covariance structure of floral traits in four species of Rosaceae were examined. The intensity of natural selection acting on floral phenotypic integration was also estimated and the available evidence regarding the magnitude of floral integration reviewed. The species studied had similar degrees of floral integration, although significant differences were observed in their variance-covariance structure. Selection acted on subsets of floral traits (i.e. selection on intrafloral integration) rather than on the integration of the whole flower. Average integration was 20% and similar to the estimated mean value of flowering plants. The review indicated that flowering plants present lower integration than expected by chance. Numerical simulations suggest that this pattern may result from selection favouring intrafloral integration. Phenotypic integration at the flower level seems to have a low adaptive value among the species surveyed. Moreover, it is proposed that pollinator-mediated selection promotes the evolution of intrafloral integration.     

Differences in pollinator faunas may generate geographic differences in floral morphology and integration in Narcissus papyraceus (Amaryllidaceae)

Pollinators may generate selective pressures that affect covariation patterns of multiple traits as well as the mean values of single floral morphological traits. Berg predicted that flowers pollinated by animals whose morphology closely matches the flower's shape will be phenotypically more integrated (tighter correlation of flower traits) than will flowers pollinated by animals not closely fitting the floral morphology. We tested this hypothesis by comparing, in the Strait of Gibraltar region (south Spain, northern Morocco), populations of Narcissus papyraceus that have geographical differences in pollinator faunas. Long-tongued, nectar-feeding moths dominate the pollinator faunas of those populations close to the Strait of Gibraltar, whereas short-tongued, pollen-feeding syrphid flies dominate in peripheral populations farther from the Strait. Populations pollinated by moths and flies differed in the mean values of several floral traits, consistent with the evolution of regional pollination ecotypes. Populations pollinated by moths showed stronger intercorrelation (floral integration) than populations pollinated by hoverflies. Moth-pollinated populations also showed less variation in flower traits than vegetative traits, and this difference was stronger than in fly-pollinated populations. Thus, the pattern of differences in the phenotypic architecture of the Narcissus flowers is consistent with the hypothesis that populations have responded to different selective pressures generated by different pollinators. These data also supported most of the specific predictions of Berg's hypotheses about integration and modularity.     

INFLUENCE OF POLLINATION SPECIALIZATION AND BREEDING SYSTEM ON FLORAL INTEGRATION AND PHENOTYPIC VARIATION IN IPOMOEA

Natural selection should reduce phenotypic variation and increase integration of floral traits involved in placement of pollen grains on stigmas. In this study, we examine the role of pollinators and breeding system on the evolution of floral traits by comparing the patterns of floral phenotypic variances and covariances in 20 Ipomoea species that differ in their level of pollination specialization and pollinator dependence incorporating phylogenetic relatedness. Plants with specialized pollination (i.e., those pollinated by one functional group or by few morphospecies) displayed less phenotypic variation and greater floral integration than generalist plants. Self‐compatible species also displayed greater floral integration than self‐incompatible species. Floral traits involved in pollen placement and pick up showed less variation and greater integration than floral traits involved in pollinator attraction. Analytical models indicate that both breeding system and the number of morphospecies had significant effects on floral integration patterns although only differences in the former were significant after accounting for phylogeny. These results suggest that specialist/self‐compatible plants experience more consistent selection on floral traits than generalist/self‐incompatible plants. Furthermore, pollinators and breeding system promote integration of floral traits involved in pollen placement and pick up rather than integration of the whole flower.     

The evolution of floral signals in relation to range overlap in a clade of California Jewelflowers (Streptanthus s.l.)

Because of their function as reproductive signals in plants, floral traits experience distinct selective pressures related to their role in speciation, reinforcement, and prolonged coexistence with close relatives. However, few studies have investigated whether population‐level processes translate into detectable signatures at the macroevolutionary scale. Here, we ask whether patterns of floral trait evolution and range overlap across a clade of California Jewelflowers reflect processes hypothesized to shape floral signal differentiation at the population level. We found a pattern of divergence in floral scent composition across the clade such that close relatives had highly disparate floral scents given their age. Accounting for range overlap with close relatives explained additional variation in floral scent over time, with sympatric species pairs having diverged more than allopatric species pairs given their age. However, three other floral traits (flower size, scent complexity and flower color) did not fit these patterns, failing to deviate from a null Brownian motion model of evolution. Together, our results suggest that selection for divergence among close relatives in the composition of floral scents may play a key, sustained role in mediating speciation and coexistence dynamics across this group, and that signatures of these dynamics may persist at the macroevolutionary scale.     

Patterns of contemporary phenotypic selection and flower integration in the hummingbird‐pollinated Nicotiana glauca between populations with different flower–pollinator combinations

We studied six populations of the hummingbird‐pollinated Nicotiana glauca to determine if the marked differences in the degree of floral‐pollinator mismatch between populations promote divergences in the pattern of pollinator‐mediated phenotypic selection on single traits and on the evolution of complexes of many interacting floral traits. We found evidence that flower phenotype is being shaped by pollinator‐mediated phenotypic selection, since corolla length was consistently under contemporary directional or stabilizing selection. Weak directional selection for longer corollas was found in two populations with low flower–pollinator mismatch; much stronger directional selection was detected for shorter corollas in two populations with high flower–pollinator mismatch; finally, the remaining two populations with intermediate flower–pollinator mismatch showed stabilizing selection for corolla length. N. glauca populations differed in every flower character measured but variations in pollinator‐mediated selection among populations were only observed for corolla length. Multiple covariation among traits was favoured, as suggested by the predominately functional patterns of integration and selection of complexes of many interacting floral traits. This was consistent with the patterns of correlational selection exhibited by four of the six populations, where corolla length was under significant selection in combination with corolla width, style length or stamen length. Overall floral integration was relatively high in all populations but phenotypic integration patterns were not clearly accounted by the degree of flower–pollinator mismatch or type of phenotypic selection, suggesting that trait covariation at the entire flower level is not explained by the current scenario of pollinator‐mediated selection.     

Evolutionary transition between bee pollination and hummingbird pollination in Salvia: Comparing means,variances and covariances of corolla traits

Covariation among traits can modify the evolutionary trajectory of complex structures. This process is thought to operate at a microevolutionary scale, but its long‐term effects remain controversial because trait covariation can itself evolve. Flower morphology, and particularly floral trait (co)variation, has been envisioned as the product of pollinator‐mediated selection. Available evidence suggests that major changes in pollinator assemblages may affect the joint expression of floral traits and their phenotypic integration. We expect species within a monophyletic lineage sharing the same pollinator type will show not only similarity in trait means but also similar phenotypic variance‐covariance structures. Here, we tested this expectation using eighteen Salvia species pollinated either by bees or by hummingbirds. Our findings indicated a nonsignificant multivariate phylogenetic signal and a decoupling between means and variance‐covariance phenotypic matrices of floral traits during the evolution to hummingbird pollination. Mean trait value analyses revealed significant differences between bee‐ and hummingbird‐pollinated Salvia species although fewer differences were detected in the covariance structure between groups. Variance‐covariance matrices were much more similar among bee‐ than hummingbird‐pollinated species. This pattern is consistent with the expectation that, unlike hummingbirds, bees physically manipulate the flower, presumably exerting stronger selection pressures favouring morphological convergence among species. Overall, we conclude that the evolution of hummingbird pollination proceeded through different independent transitions. Thus, although the evolution of hummingbird pollination led to a new phenotypic optimum, the process involved the diversification of the covariance structure.     

Floral integration,phenotypic covariance structure and pollinator variation in bumblebee‐pollinated Helleborus foetidus

By analysing patterns of phenotypic integration and multivariate covariance structure of five metric floral traits in nine Iberian populations of bumblebee‐pollinated Helleborus foetidus (Ranunculaceae), this paper attempts to test the general hypothesis that pollinators enhance floral integration and selectively modify phenotypic correlations between functionally linked floral traits. The five floral traits examined exhibited significant phenotypic integration at all populations, and both the magnitude and the pattern of integration differed widely among populations. Variation in extent and pattern of integration was neither distance‐dependent nor significantly related to between‐population variation in taxonomical composition and morphological diversity of the pollinator assemblage. Patterns of floral integration were closer to expectations derived from consideration of developmental affinities between floral whorls than to expectations based on a pollinator‐mediated adaptive hypothesis. Taken together, results of this study suggest that between‐population differences in magnitude and pattern of floral integration in H. foetidus are probably best explained as a consequence of random genetic sampling in the characteristically small and ephemeral populations of this species, rather than reflecting the selective action of current pollinators.     

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.     

Correlated morphological and colour differences among females of the damselfly Ischnura elegans

Abstract 1. The female‐limited colour polymorphic damselfly Ischnura elegans has proven to be an interesting study organism both as an example of female sexual polymorphism, and in the context of the evolution of colour polymorphism, as a model of speciation processes. 2. Previous research suggests the existence of correlations between colour morph and other phenotypic traits, and the different female morphs in I. elegans may be pursuing alternative phenotypically integrated strategies. However, previous research on morphological differences in southern Swedish individuals of this species was only carried out on laboratory‐raised offspring from a single population, leaving open the question of how widespread such differences are. 3. The present study therefore analysed multi‐generational data from 12 populations, investigating morphological differences between the female morphs in the field, differences in the pattern of phenotypic integration between morphs, and quantified selection on morphological traits. 4. It was found that consistent morphological differences indeed existed between the morphs across populations, confirming that the previously observed differences were not simply a laboratory artefact. It was also found, somewhat surprisingly, that despite the existence of sexual dimorphism in body size and shape, patterns of phenotypic integration differed most between the morphs and not between the sexes. Finally, linear selection gradients showed that female morphology affected fecundity differently between the morphs. 5. We discuss the relevance of these results to the male mimicry hypothesis and to the existence of potential ecological differences between the morphs.     

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.     

Multivariate phenotypes and the potential for alternative phenotypic optima in wall lizard (Podarcis muralis) ventral colour morphs

A major goal in evolutionary biology is to determine how phenotypic variation arises and is maintained in natural populations. Recent studies examining the morphological, physiological and behavioural differences among discrete colour morphotypes (morphs) have revealed several mechanisms that maintain discrete variation within populations, including frequency‐dependence, density‐dependence and correlational selection. For example, trade‐offs over resource allocation to morphological, physiological and behavioural traits can drive correlational selection for morph‐specific phenotypic optima. Here, we describe a ventral colour polymorphism in the wall lizard (Podarcis muralis) and test the hypothesis that morphs differ along multivariate axes defined by trade‐offs in morphological, physiological, and immunological traits. We show that ventral colour is a discrete trait and that morphs differ in body size, prevalence of infection by parasites and infection intensity. We also find that morphs differ along multivariate phenotypic axes and experience different multivariate selection pressures. Our results suggest that multivariate selection pressures may favour alternative optimal morph‐specific phenotypes in P. muralis.     

Contrasting Mode of Evolution at a Coat Color Locus in Wild and Domestic Pigs

Despite having only begun ~10,000 years ago, the process of domestication has resulted in a degree of phenotypic variation within individual species normally associated with much deeper evolutionary time scales. Though many variable traits found in domestic animals are the result of relatively recent human-mediated selection, uncertainty remains as to whether the modern ubiquity of long-standing variable traits such as coat color results from selection or drift, and whether the underlying alleles were present in the wild ancestor or appeared after domestication began. Here, through an investigation of sequence diversity at the porcine melanocortin receptor 1 (MC1R) locus, we provide evidence that wild and domestic pig (Sus scrofa) haplotypes from China and Europe are the result of strikingly different selection pressures, and that coat color variation is the result of intentional selection for alleles that appeared after the advent of domestication. Asian and European wild boar (evolutionarily distinct subspecies) differed only by synonymous substitutions, demonstrating that camouflage coat color is maintained by purifying selection. In domestic pigs, however, each of nine unique mutations altered the amino acid sequence thus generating coat color diversity. Most domestic MC1R alleles differed by more than one mutation from the wild-type, implying a long history of strong positive selection for coat color variants, during which time humans have cherry-picked rare mutations that would be quickly eliminated in wild contexts. This pattern demonstrates that coat color phenotypes result from direct human selection and not via a simple relaxation of natural selective pressures.     

MULTIYEAR STUDY OF MULTIVARIATE LINEAR AND NONLINEAR PHENOTYPIC SELECTION ON FLORAL TRAITS OF HUMMINGBIRD-POLLINATED SILENE VIRGINICA

Pollination syndromes suggest that convergent evolution of floral traits and trait combinations reflects similar selection pressures. Accordingly, a pattern of selection on floral traits is expected to be consistent with increasing the attraction and pollen transfer of the important pollinator. We measured individual variation in six floral traits and yearly and lifetime total plant seed and fruit production of 758 plants across nine years of study in natural populations of Ruby-Throated Hummingbird-pollinated Silene virginica. The type, strength, and direction of selection gradients were observed by year, and for two cohorts selection was estimated through lifetime maternal fitness. Positive directional selection was detected on floral display height in all years of study and stigma exsertion in all years but one. Significant quadratic and correlational selection gradients were rare. However, a canonical analysis of the gamma matrix indicated nonlinear selection was common; if significant curvature was detected it was convex with one exception. Our analyses demonstrated selection favored trait combinations and the integration of floral features of attraction and pollen transfer efficiency that were consistent with the hummingbird pollination syndrome.     

Phenotypic plasticity in insects: the effects of substrate color on the coloration of two ground-hopper species

SUMMARY The question of how phenotypic variation is maintained within populations has long been a central issue in evolutionary biology. Most of these studies focused on the maintenance of genetic variability, but the phenotype of organisms may also be influenced by environmental cues experienced during ontogeny. Color polymorphism has received particular attention in evolutionary studies as it has strong fitness consequences. However, if body coloration is influenced by the environment, any conclusions on evolutionary consequences of fitness trade-offs can be misleading. Here we present data from a laboratory experiment on the influence of substrate color on three aspects of the coloration of two ground-hopper species, Tetrix subulata and Tetrix ceperoi . We reared hatchlings either on dark or on light substrates, using a split-brood design. Although the type of pronotal pattern changed mainly in response to nymphal development, the basic color was strongly influenced by the substrate color. In both species, black and dark olive color morphs were found more frequently on the dark substrate, whereas the gray color morph dominated on the light substrate. These findings have considerable implications for our understanding of color morph evolution as they show that color polymorphism may not only be maintained by natural selection acting on discrete color morphs, but also by phenotypic plasticity, which enables organisms to adjust to the environmental conditions experienced during ontogeny. This facultative morphology is opposing to the prevailing view of color morph adaptation, which assumes a purely genetic determination and co-evolution of discrete color morphs with life history traits.     

Pervasive genetic integration directs the evolution of human skull shape

It has long been unclear whether the different derived cranial traits of modern humans evolved independently in response to separate selection pressures or whether they resulted from the inherent morphological integration throughout the skull. In a novel approach to this issue, we combine evolutionary quantitative genetics and geometric morphometrics to analyze genetic and phenotypic integration in human skull shape. We measured human skulls in the ossuary of Hallstatt (Austria), which offer a unique opportunity because they are associated with genealogical data. Our results indicate pronounced covariation of traits throughout the skull. Separate simulations of selection for localized shape changes corresponding to some of the principal derived characters of modern human skulls produced outcomes that were similar to each other and involved a joint response in all of these traits. The data for both genetic and phenotypic shape variation were not consistent with the hypothesis that the face, cranial base, and cranial vault are completely independent modules but relatively strongly integrated structures. These results indicate pervasive integration in the human skull and suggest a reinterpretation of the selective scenario for human evolution where the origin of any one of the derived characters may have facilitated the evolution of the others.     

Selection by Pollinators on Floral Traits in Generalized Trollius ranunculoides (Ranunculaceae) along Altitudinal Gradients

Abundance and visitation of pollinator assemblages tend to decrease with altitude, leading to an increase in pollen limitation. Thus increased competition for pollinators may generate stronger selection on attractive traits of flowers at high elevations and cause floral adaptive evolution. Few studies have related geographically variable selection from pollinators and intraspecific floral differentiation. We investigated the variation of Trollius ranunculoides flowers and its pollinators along an altitudinal gradient on the eastern Qinghai-Tibet Plateau, and measured phenotypic selection by pollinators on floral traits across populations. The results showed significant decline of visitation rate of bees along altitudinal gradients, while flies was unchanged. When fitness is estimated by the visitation rate rather than the seed number per plant, phenotypic selection on the sepal length and width shows a significant correlation between the selection strength and the altitude, with stronger selection at higher altitudes. However, significant decreases in the sepal length and width of T. ranunculoides along the altitudinal gradient did not correspond to stronger selection of pollinators. In contrast to the pollinator visitation, mean annual precipitation negatively affected the sepal length and width, and contributed more to geographical variation in measured floral traits than the visitation rate of pollinators. Therefore, the sepal size may have been influenced by conflicting selection pressures from biotic and abiotic selective agents. This study supports the hypothesis that lower pollinator availability at high altitude can intensify selection on flower attractive traits, but abiotic selection is preventing a response to selection from pollinators.     

Morph‐specific selection on floral traits in a polymorphic plant

Correlations between phenotypic traits are common in many organisms, but the relative importance of nonadaptive mechanisms and selection for the evolution and maintenance of such correlations are poorly understood. In polymorphic species, morphs may evolve quantitative differences in additional characters as a result of morph‐specific selection. The perennial rosette herb Primula farinosa is polymorphic for scape length. The short‐scaped morph is less damaged by grazers and seed predators but is more strongly pollen limited than the long‐scaped morph. We examined whether morph‐specific differences in biotic interactions are associated with differences in selection on two other traits affecting floral display (number of flowers and petal size) and on one trait likely to affect pollination efficiency (corolla tube width) in three P. farinosa populations. Differences in selection between morphs were detected in one population. In this population, selection for more flowers and larger petals was stronger in the short‐scaped than in the long‐scaped morph, and although there was selection for narrower corolla tubes in the short‐scaped morph, no statistically significant selection on corolla tube width could be detected in the long‐scaped morph. In the study populations, the short‐scaped morph produced more and larger flowers and wider corolla tubes. Current morph‐specific selection was thus only partly consistent with trait differences between morphs. The results provide evidence of morph‐specific selection on traits associated with floral display and pollination efficiency, respectively.     

Island biology and morphological divergence of the Skyros wall lizard <Emphasis Type="Italic">Podarcis gaigeae</Emphasis>: a combined role for local selection and genetic drift on color morph frequency divergence?

Background  

Patterns of spatial variation in discrete phenotypic traits can be used to draw inferences about the adaptive significance of traits and evolutionary processes, especially when compared to patterns of neutral genetic variation. Population divergence in adaptive traits such as color morphs can be influenced by both local ecology and stochastic factors such as genetic drift or founder events. Here, we use quantitative color measurements of males and females of Skyros wall lizard, Podarcis gaigeae, to demonstrate that this species is polymorphic with respect to throat color, and the morphs form discrete phenotypic clusters with limited overlap between categories. We use divergence in throat color morph frequencies and compare that to neutral genetic variation to infer the evolutionary processes acting on islet- and mainland populations.