Floral Integration Research Articles

Patterns of phenotypic correlations among morphological traits across plants and animals.

Despite the long-standing interest of biologists in patterns of correlation and phenotypic integration, little attention has been paid to patterns of correlation across a broad phylogenetic spectrum. We report analyses of mean phenotypic correlations among a variety of linear measurements from a wide diversity of plants and animals, addressing questions about function, development, integration and modularity. These analyses suggest that vertebrates, hemimetabolous insects and vegetative traits in plants have similar mean correlations, around 0.5. Traits of holometabolous insects are much more highly correlated, with a mean correlation of 0.84; this may be due to developmental homeostasis caused by lower spatial and temporal environmental variance during complete metamorphosis. The lowest mean correlations were those between floral and vegetative traits, consistent with Berg's ideas about functional independence between these modules. Within trait groups, the lowest mean correlations were among vertebrate head traits and floral traits (0.38-0.39). The former may be due to independence between skull modules. While there is little evidence for floral integration overall, certain sets of functionally related floral traits are highly integrated. A case study of the latter is described from wild radish flowers.

The search for Pleiades in trait constellations: functional integration and phenotypic selection in the complex flowers of Morrenia brachystephana (Apocynaceae)

Pollinator-mediated natural selection on single traits, such as corolla tube or spur length, has been well documented. However, flower phenotypes are usually complex, and selection is expected to act on several traits that functionally interact rather than on a single isolated trait. Despite the fact that selection on complex phenotypes is expectedly widespread, multivariate selection modelling on such phenotypes still remains under-explored in plants. Species of the subfamily Asclepiadoideae (Apocynaceae) provide an opportunity to study such complex flower contrivances integrated by fine-scaled organs from disparate developmental origin. We studied the correlation structure among linear floral traits (i) by testing a priori morphological, functional or developmental hypotheses among traits and (ii) by exploring the organization of flower covariation, considering alternative expectations of modular organization or whole flower integration through conditional dependence analysis (CDA) and integration matrices. The phenotypic selection approach was applied to determine whether floral traits involved in the functioning of the pollination mechanism were affected by natural selection. Floral integration was low, suggesting that flowers are organized in more than just one correlation pleiad; our hypothetical functional correlation matrix was significantly correlated with the empirical matrix, and the CDA revealed three putative modules. Analyses of phenotypic selection showed significant linear and correlational gradients, lending support to expectations of functional interactions between floral traits. Significant correlational selection gradients found involved traits of different floral whorls, providing evidence for the existence of functional integration across developmental domains.

Phenological associations of within‐ and among‐plant variation in gender with floral morphology and integration in protandrous Delphinium glaucum

Summary1. Flowering‐time differences within and among protandrous, hermaphroditic plants shift the floral sex ratio from male‐ to female‐dominated during a population’s flowering season. This dynamic should induce negative frequency‐dependent selection favouring relatively greater investment of resources and time in female function by early flowers and early‐flowering plants than by late flowers and late‐flowering individuals. In contrast, selection for floral integration to facilitate pollen export and import should limit floral variation.2. We assessed these contrasting expectations for the protandrous Delphinium glaucum by considering the relation of variation and covariation in the lengths of perianth segments, anther and ovule number, and male‐ and female‐phase duration for flowers at three positions within inflorescences to the first flowering date, mean gender and size of 34 plants.3. Reproductive phenotypes varied among and within plants in association with a shift in population floral sex ratio from male‐ to female‐biased, but not with plant size. Early‐flowering plants had female‐biased phenotypic gender and smaller flowers with fewer anthers per ovule and shorter male phases than late‐flowering plants. Within individuals, earlier (lower) flowers were larger with higher female effort, in terms of both the relative production of ovules and anthers and the relative durations of female and male phases, than later (upper) flowers. Overall, these results are more consistent with the expectations of negative frequency‐dependent selection than with proximate resource allocation.4. Correlations among floral traits indicated significant floral integration. However, these correlations weakened from lower to upper flowers, suggesting that the patterns of intra‐individual variation limit the extent of integration.5. Synthesis. Reproductive phenotypes that incorporate systematic among‐flower variation and vary consistently among individuals with flowering time, such as those exhibited by D. glaucum, may be typical of dichogamous species with multi‐flowered inflorescences. Such diversity within and among plants should result from a combination of density‐dependent selection against simultaneous flowering of individuals and frequency‐dependent selection favouring emphasis on the least common sex role during specific stages of the flowering season, both facilitated by the positive assortative mating that accompanies asynchronous flowering among individuals.

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.

Modular genetic architecture of floral morphology inNicotiana: quantitative genetic and comparative phenotypic approaches to floral integration

Animal-pollinated flowers are complex structures that may require a precise configuration of floral organs for proper function. As such, they represent an excellent system with which we can examine the role of phenotypic integration and modularity in morphological evolution. We use complementary quantitative genetic and comparative phenotypic approaches to examine correlations among floral characters in Nicotiana alata, N. forgetiana and their artificial fourth-generation hybrids. Flowers of both species share basic patterns of genetic and phenotypic correlations characterized by at least two integrated character suites that are relatively independent of each other and are not disrupted by four generations of recombination in hybrids. We conclude that these integrated character suites represent phenotypic modules that are the product of a modular genetic architecture. Intrafloral modularity may have been critical for rapid specialization of these species to different pollinators.

Patterns of style polymorphism in five species of the South African genus Nivenia (Iridaceae)

Heterostylous plants have been characterized by the presence of two or three discrete morphs that differ in their sex organ position within populations. This polymorphism is widely distributed among the angiosperms, but detailed studies are limited to few taxonomic groups. Although a small representation, evolutionary meaningful variations of the heterostylous syndrome have been reported when precise measurements of the sexual whorls were taken. A thorough exploration of groups where heterostyly has been reported should offer new opportunities to further testing the evolutionary hypotheses explaining heterostyly. Here, the traits defining heterostyly were explored in half of the species in Nivenia, the only genus of Iridiaceae where heterostyly has been reported. Detailed morphometric analysis of the flower sexual whorls and some traits considered as ancillary are supplied to determine for each population (a) the kind of stylar polymorphism, (b) the morph ratio and (c) the degree of reciprocity between sexual whorls. Also the rates of assortative (within morph) versus disassortative (between morphs) pollen transfer were estimated by analysing pollen loads on stigmas. The association between floral phenotypic integration and the reciprocity between sexual whorls was estimated; both characteristics have been quoted as dependent on the accuracy of the fit between pollinators and flowers and therefore related to the efficiency of pollen transfer. Different types of polymorphism, differing in their degree of reciprocity, were found in Nivenia. Effective disassortative mating appears to be common, since (a) all dimorphic populations show equal morph-ratios (isoplethy), and (b) the pollen placed on the stigmas of each morph is likely to be coming from the other (complementary) morph. The most reciprocal populations of the heterostylous species have also the highest values of phenotypical integration. Stigma height dimorphism, as opposed to distyly, is proven for the first time in Nivenia. The presence of different types of polymorphism within the genus is consistent with hypotheses of the evolution of heterostyly. The role of the pollinators as the leading force of the transition seems to be apparent, since floral integration is related to reciprocity.

Patterns of contemporary phenotypic selection and flower integration in the hummingbird-pollinatedNicotiana glaucabetween 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.

Changes in sexual organ reciprocity and phenotypic floral integration during the tristyly–distyly transition inOxalis alpina

Although the 6 magnitude and pattern of correlation among floral traits (phenotypic integration) is usually conceived as an adaptation for successful pollination and reproduction, studies on the evolution of plant reproductive systems have generally focused on one or a few characters. If evolutionary transitions between reproductive systems involve morphological floral adjustments, changes in the magnitude and pattern of phenotypic integration of floral traits may be expected. In this study, we focused on the evolutionary dynamics of a complex adaptive trait, the extent of reciprocity (reciprocal placement) among sexual organs in a heterostylous species, and explored the associated changes in phenotypic floral integration during the transition from tristyly to distyly. The extent of reciprocity and both the magnitude and pattern of floral integration were characterized in 12 populations of Oxalis alpina representing the tristyly-distyly gradient. Although the extent of reciprocity increased along the tristyly-distyly transition, the flower size diminished. These adjustments did not affect the magnitude, but did affect the pattern, of floral integration. *Changes in the pattern of floral integration suggested that allometric, functional and pleiotropic relationships among floral traits were affected during this evolutionary transition.

Darwinism renewed: contemporary studies of plant adaptation

Darwinism renewed: contemporary studies of plant adaptation

Macroevolutionary patterns of pollination accuracy: a comparison of three genera

We hypothesize that pollination efficiency selects for equal distances between the pollinator reward and the anthers, and the stigmas, creating an adaptive ridge. We predict that this fitness surface governs the divergence of many plant species. We use the theory of adaptive accuracy, precision and mean optimality to assess how close populations lie to the hypothesized adaptive ridge and which factors contribute to departure from the optimum. Patterns of accuracy of pollen placement and receipt were compared across species in three study systems, Dalechampia (Euphorbiaceae), Collinsieae (Plantaginaceae) and Stylidium (Stylidiaceae), in order to assess the roles of stamen/stigma imprecision and population mean departure from the optimum in the generation of floral inaccuracy. We found that population mean departure from the optimum was the most important factor in Dalechampia, female imprecision and departure from the optimum were about equally important factors in Collinsieae, and stamen and stigma imprecision were equally important in Stylidium, with virtually no departure from the optimum. Possible reasons for imprecision and departure from the optimum were assessed using phylogenetically informed methods, indicating important roles of limited floral integration in the generation of imprecision, and conflicting selective pressures, associated with outcrossing, in the generation of departure from the optimum.

Implications of a long-term, pollinator-mediated selection on floral traits in a generalist herb

The phenotypic selection of a diverse insect assemblage was studied on a generalist plant species (Paeonia broteroi) in ten flowering seasons, with tests for whether visitor preferences for plants with larger flowers eventually translated into significant differences among plants in visitation rates, seed production, seed mass, seed germination and seedling survival. Selection gradients were used to assess if selection on flower size contributed to explain differences in visitation rates, seed production and seed mass. First, independent analyses were carried out for each season; then for the ten season as a whole. Seedling emergence and survival were assessed by generalized linear models. Directional selection was found on flower size through visitation rates and seed production, and stabilizing selection through seed mass. Thus, larger flowers were more visited, and produced more, but lighter seeds, than smaller flowers. The results suggest a conflicting selection on flower size through seed number and size. Floral integration found in the study populations was larger than that in populations of a distant region. Finally, seed size did not influence seedling emergence and survival; thus, any advantages of seed size may be constrained under natural conditions before plants become reproductive individuals. Plants with larger flowers may be benefited by producing more lighter seeds than fewer heavier ones, as they may contribute disproportionately to the seed bank, and have better chances that any descendant could eventually recruit. However, it seems unlikely that differences in flower size and integration found among populations in different regions could have been originated by rapid evolutionary change. First, because of the conflicting selection described; second, because of the remarkably low seedling survival found under natural conditions. Consequently, the influence of pollinator selection alone does not seem to explain differences in flower size and integration.

Questions about floral (dis)integration

Questions about floral (dis)integration

Using phenotypic manipulations to study multivariate selection of floral trait associations

A basic theme in the study of plant-pollinator interactions is that pollinators select not just for single floral traits, but for associations of traits. Responses of pollinators to sets of traits are inherent in the idea of pollinator syndromes. In its most extreme form, selection on a suite of traits can take the form of correlational selection, in which a response to one trait depends on the value of another, thereby favouring floral integration. Despite the importance of selection for combinations of traits in the evolution of flowers, evidence is relatively sparse and relies mostly on observational approaches. Here, methods for measuring selection on multivariate suites of floral traits are presented, and the studies to date are reviewed. It is argued that phenotypic manipulations present a powerful, but rarely used, approach to teasing apart the separate and combined effects of particular traits. The approach is illustrated with data from studies of alpine plants in Colorado and New Zealand, and recommendations are made about several features of the design of such experiments. Phenotypic manipulations of two or more traits in combination provide a direct way of testing for selection of floral trait associations. Such experiments will be particularly valuable if rooted in hypotheses about differences between types of pollinators and tied to a proposed evolutionary history.

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.

How little is too little? The adaptive value of floral integration

For more than a century the idea that natural selection favors high levels of floral integration has prevailed as a paradigm among floral biologists. However, there is very little empirical evidence of the adaptive value of floral integration. In this addendum we highlight an important result derived from an empirical study complemented with a literature review and mathematical simulations. Results indicated that intrafloral integration but not floral integration was selected among four species of Rosaceae. The literature review coupled with null models revealed that flowering plants have on average lower than expected levels of floral integration. Mathematical simulations further demonstrated that observed levels of floral integration might result from selection favoring increased intrafloral integration. Altogether, these findings suggest that in most flowering plants, floral integration has a low adaptive value and could be a by-product of selection favoring intrafloral integration.

Differences in pollinator faunas may generate geographic differences in floral morphology and integration inNarcissus 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 ofNarcissus papyraceusthat 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 theNarcissusflowers 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.

Phylogenetic analysis of floral integration inSchizanthus(Solanaceae): does pollination truly integrate corolla traits?

To assess whether floral integration patterns result from the action of pollinator selection on functionally related traits, we compared corolla integration patterns in eight Schizanthus species differing in pollination systems and in their degree of pollinator dependence across a molecular phylogeny. Integration patterns differed among species and these differences were not related to their phylogenetic relatedness. When the putative original function of some corolla traits was lost in pollinator-dependent species, the integration among nonfunctional characters and the rest of the corolla traits was disrupted. This pattern was not presented in species adapted for late autonomous selfing, which exhibited higher corolla integration than their pollinator-dependent relatives. These results suggest that corolla integration in pollinator-dependent species was shaped by pollinator-mediated selection. Decoupling of nonfunctional traits in these species may result from a relaxation of correlational selection or from selection acting against a default covariation provided by genetic and developmental connections.

Relaxed pollinator‐mediated selection weakens floral integration in self‐compatible taxa ofLeavenworthia(Brassicaceae)

Natural selection should favor the integration of floral traits that enhance pollen export and import in plant populations that rely upon pollinators. If this is true, then phenotypic correlations between floral traits should weaken in self-fertilizing groups that do not require pollinator visitation to produce seed. We tested this hypothesis in Leavenworthia, a plant genus in which there have been multiple independent losses of the sporophytic self-incompatibility system found throughout the Brassicaceae. In particular, we conducted phylogenetically independent contrasts of floral trait correlations between two pairs of self-incompatible (SI) and self-compatible (SC) sister taxa. In support of the hypothesis that pollinator-mediated selection integrates floral traits, we found that both SC Leavenworthia taxa have weaker overall floral correlations in comparison to sister taxa that rely upon pollinators. The two independently derived SC Leavenworthia flowers have significantly weaker stamen-petal or pistil-petal correlations, respectively, whereas the stamen-pistil correlation remains constant. These patterns suggest that relaxation of pollinator-mediated selection weakens the integration of traits associated with pollen export and import. The retention of high stamen-pistil correlations in the SC taxa of Leavenworthia further implies that the integration of these traits is either constrained or maintained by selection favoring the successful transfer of pollen within flowers to secure self-pollination.

Genetic constraints on floral evolution: a review and evaluation of patterns

The characteristics of flowers influence most aspects of angiosperm reproduction, including the agents of pollination and patterns of mating. Thus, a clear view of the forces that mediate floral phenotypic evolution is central to understanding angiosperm diversity. Here, we inform on the capacity for floral phenotype to respond to selection by reviewing published data on heritabilities and genetic correlations for several classes of floral traits (primary sexual, attraction, mating system) in hermaphroditic plants. We find significant heritability for all floral traits but also variation among them, as well as a tendency for heritability to vary with mating system, but not life history. We additionally test predictions stemming from life history theory (eg, negative covariation between male-female traits and flower size-flower number), and ideas concerning the extent and pattern of genetic integration between flowers and leaves, and between the sexes of dioecious and gynodioecious species. We find mixed evidence for life history tradeoffs. We find strong support for floral integration and its relation with floral morphology (actinomorphy vs zygomorphy) and for a decoupling of floral and vegetative traits, but no evidence that modular integration varies with floral morphology. Lastly, we find mixed evidence for a relationship between the level of sexual dimorphism in attraction traits and the between-sex correlation in gender dimorphic plants.

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

Abstract 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.