Selection on floral traits through male fertility in a natural plant population

Most studies on selection in plants estimate female fitness components and neglect male mating success, although the latter might also be fundamental to understand adaptive evolution. Information from molecular genetic markers can be used to assess determinants of male mating success through parentage analyses. We estimated paternal selection gradients on floral traits in a large natural population of the herb Mimulus guttatus using a paternity probability model and maximum likelihood methods. This analysis revealed more significant selection gradients than a previous analysis based on regression of estimated male fertilities on floral traits. There were differences between results of univariate and multivariate analyses most likely due to the underlying covariance structure of the traits. Multivariate analysis, which corrects for the covariance structure of the traits, indicated that male mating success declined with distance from and depended on the direction to the mother plants. Moreover, there was directional selection for plants with fewer open flowers which have smaller corollas, a smaller anther-stigma separation, more red dots on the corolla and a larger fluctuating asymmetry therein. For most of these traits, however, there was also stabilizing selection indicating that there are intermediate optima for these traits. The large number of significant selection gradients in this study shows that even in relatively large natural populations where not all males can be sampled, it is possible to detect significant paternal selection gradients, and that such studies can give us valuable information required to better understand adaptive plant evolution.

Pollinator responses to variation in floral display and flower size in dioecious Sagittaria latifolia (Alismataceae)

In animal-pollinated plants with unisexual flowers, sexual dimorphism in floral traits may be the consequence of pollinator-mediated selection. Experimental investigations of the effects of variation in flower size and floral display on pollinator visitation can provide insights into the evolution of floral dimorphism in dioecious plants. Here, we investigated pollinator responses to experimental arrays of dioecious Sagittaria latifolia in which we manipulated floral display and flower size. We also examined whether there were changes in pollinator visitation with increasing dimorphism in flower size. In S. latifolia, males have larger flowers and smaller floral displays than females. Visitation by pollinators, mainly flies and bees, was more frequent for male than for female inflorescences and increased with increasing flower size, regardless of sex. The number of insect visits per flower decreased with increasing floral display in males but remained constant in females. Greater sexual dimorphism in flower size increased visits to male inflorescences but had no influence on the number of visits to female inflorescences. These results suggest that larger flower sizes would be advantageous to both females and males, and no evidence was found that females suffer from increased flower-size dimorphism. Small daily floral displays may benefit males by allowing extended flowering periods and greater opportunities for effective pollen dispersal.

Dissection of floral pollination syndromes in petunia

Animal-mediated pollination is essential in the reproductive biology of many flowering plants and tends to be associated with pollination syndromes, sets of floral traits that are adapted to particular groups of pollinators. The complexity and functional convergence of various traits within pollination syndromes are outstanding examples of biological adaptation, raising questions about their mechanisms and origins. In the genus Petunia, complex pollination syndromes are found for nocturnal hawkmoths (P. axillaris) and diurnal bees (P. integrifolia), with characteristic differences in petal color, corolla shape, reproductive organ morphology, nectar quantity, nectar quality, and fragrance. We dissected the Petunia syndromes into their most important phenotypic and genetic components. They appear to include several distinct differences, such as cell-growth and cell-division patterns in the basal third of the petals, elongation of the ventral stamens, nectar secretion and nectar sugar metabolism, and enzymatic differentiation in the phenylpropanoid pathway. In backcross-inbred lines of species-derived chromosome segments in a transposon tagging strain of P. hybrida, one to five quantitative trait loci were identified for each syndrome component. Two loci for stamen elongation and nectar volume were confirmed in introgression lines and showed large allelic differences. The combined data provide a framework for a detailed understanding of floral syndromes from their developmental and molecular basis to their impact on animal behavior. With its molecular genetic tools, this Petunia system provides a novel venue for a pattern of adaptive radiation that is among the most characteristic of flowering plants.

MYB-FL controls gain and loss of floral UV absorbance, a key trait affecting pollinator preference and reproductive isolation

Adaptations to new pollinators involve multiple floral traits, each requiring coordinated changes in multiple genes. Despite this genetic complexity, shifts in pollination syndromes have happened frequently during angiosperm evolution. Here we study the genetic basis of floral UV absorbance, a key trait for attracting nocturnal pollinators. In Petunia, mutations in a single gene, MYB-FL, explain two transitions in UV absorbance. A gain of UV absorbance in the transition from bee to moth pollination was determined by a cis-regulatory mutation, whereas a frameshift mutation caused subsequent loss of UV absorbance during the transition from moth to hummingbird pollination. The functional differences in MYB-FL provide insight into the process of speciation and clarify phylogenetic relationships between nascent species.

Adaptive rather than non-adaptive evolution of Mimulus guttatus in its invasive range

Adaptive and non-adaptive evolutionary processes are likely to play important roles in biological invasions but their relative importance has hardly ever been quantified. Moreover, although genetic differences between populations in their native versus invasive ranges may simply reflect different positions along a genetic latitudinal cline, this has rarely been controlled for. To study non-adaptive evolutionary processes in invasion of Mimulus guttatus, we used allozyme analyses on offspring of seven native populations from western North America, and three and four invasive populations from Scotland and New Zealand, respectively. To study quantitative genetic differentiation, we grew 2474 plants representing 17 native populations and the seven invasive populations in a common greenhouse environment under temporarily and permanently wet soil conditions. The absence of allozyme differentiation between the invasive and native range indicates that multiple genotypes had been introduced to Scotland and New Zealand, and suggests that founder effects and genetic drift played small, if any, roles in shaping genetic structure of invasive M. guttatus populations. Plants from the invasive and native range did not differ in phenology, floral traits and sexual and vegetative reproduction, and also not in plastic responses to the watering treatments. However, plants from the invasive range produced twice as many flower-bearing upright side branches than the ones from the native populations. Further, with increasing latitude of collection, vegetative reproduction of our experimental plants increased while sexual reproduction decreased. Plants from the invasive and native range shared these latitudinal clines. Because allozymes showed that the relatedness between native and invasive populations did not depend on latitude, this suggests that plants in the invasive regions have adapted to the local latitude. Overall, our study indicates that quantitative genetic variation of M. guttatus in its two invasive regions is shaped by adaptive evolutionary processes rather than by non-adaptive ones. (C) 2007 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Support for the predictions of the pollinator-mediated stabilizing selection hypothesis

Aims Floral traits are frequency used in traditional plant systematics because Of their assumed constancy. One potential reason for the apparent constancy of flower size is that effective pollen transfer between flowers depends oil the accuracy of the physical fit between the flower and pollinator. Therefore, dowels are likely to he under stronger stabilizing selection for uniform size than vegetative plant parts. Moreover, as predicted by the pollinator-mediated stabilizing selection (PMSS) hypothesis, all accurate fit between flowers and their pollinators is likely to he more important for specialized pollination systems as found in many species with bilaterally symmetric (zygomorphic) flowers than for species, with radially symmetric (actinomorphic) flowers. Methods In a comparative study of 15 zygomorphic and 13 actinomorphic species ill Switzerland, we tested whether variation in flower size, among and within individuals, is smaller than variation ill leaf size and whether variation in flower size is smaller ill zygomorphic compared to actinomorphic species. Important findings Indeed, variation ill leaf length was significantly larger than variation in flower length and width. Within-individual variation ill flower and leaf sizes did not differ significantly between zygomorphic and actinomorphic species. In line with the predictions of the PMSS, among-individual variation ill flower length and flower width was significantly smaller for zygomorphic species than for actinomorphic species, while the two groups did not differ in leaf length variation. This suggests that plants with zygomorphic flowers have undergone stronger selection for uniform flowers than plants with actinomorphic flowers. This supports that the uniformity of flowers compared to vegetative structures within species, as already observed in traditional plant systematics, is, at least in part, a consequence of the requirement for effective pollination.

Tight Genetic Linkage of Prezygotic Barrier Loci Creates a Multifunctional Speciation Island in Petunia

Most flowering plants depend on animal vectors for pollination and seed dispersal. Differential pollinator preferences lead to premating isolation and thus reduced gene flow between interbreeding plant populations [1, 2, 3 and 4]. Sets of floral traits, adapted to attract specific pollinator guilds, are called pollination syndromes [5]. Shifts in pollination syndromes have occurred surprisingly frequently [6], considering that they must involve coordinated changes in multiple genes affecting multiple floral traits. Although the identification of individual genes specifying single pollination syndrome traits is in progress in many species, little is known about the genetic architecture of coadapted pollination syndrome traits and how they are embedded within the genome [7]. Here we describe the tight genetic linkage of loci specifying five major pollination syndrome traits in the genus Petunia: visible color, UV absorption, floral scent production, pistil length, and stamen length. Comparison with other Solanaceae indicates that, in P. exserta and P. axillaris, loci specifying these floral traits have specifically become clustered into a multifunctional “speciation island” [ 8 and 9]. Such an arrangement promotes linkage disequilibrium and avoids the dissolution of pollination syndromes by recombination. We suggest that tight genetic linkage provides a mechanism for rapid switches between distinct pollination syndromes in response to changes in pollinator availabilities.

Color and Scent: How Single Genes Influence Pollinator Attraction

A major function of angiosperm flowers is the recruitment of animal pollinators that serve to transfer pollen among conspecific plants. Distinct sets of floral characteristics, called pollination syndromes, are correlated with visitation by specific groups of pollinators. Switches among pollination syndromes have occurred in many plant families. Such switches must have involved coordinated changes in multiple traits and multiple genes. Two well-studied floral traits affecting pollinator attraction are petal color and scent production. We review current knowledge about the biosynthetic pathways for floral color and scent production and their interaction at the genetic and biochemical levels. A key question in the field concerns the genes that underlie natural variation in color and scent and how such genes affect pollinator preference, reproductive isolation, and ultimately speciation.

The genetics of reproductive organ morphology in two Petunia species with contrasting pollination syndromes

Main conclusion Switches between pollination syndromes have happened frequently during angiosperm evolution. Using QTL mapping and reciprocal introgressions, we show that changes in reproductive organ morphology have a simple genetic basis. In animal-pollinated plants, flowers have evolved to optimize pollination efficiency by different pollinator guilds and hence reproductive success. The two Petunia species, P. axillaris and P. exserta, display pollination syndromes adapted to moth or hummingbird pollination. For the floral traits color and scent, genetic loci of large phenotypic effect have been well documented. However, such large-effect loci may be typical for shifts in simple biochemical traits, whereas the evolution of morphological traits may involve multiple mutations of small phenotypic effect. Here, we performed a quantitative trait locus (QTL) analysis of floral morphology, followed by an in-depth study of pistil and stamen morphology and the introgression of individual QTL into reciprocal parental backgrounds. Two QTLs, on chromosomes II and V, are sufficient to explain the interspecific difference in pistil and stamen length. Since most of the difference in organ length is caused by differences in cell number, genes underlying these QTLs are likely to be involved in cell cycle regulation. Interestingly, conservation of the locus on chromosome II in a different P. axillaris subspecies suggests that the evolution of organ elongation was initiated on chromosome II in adaptation to different pollinators. We recently showed that QTLs for pistil and stamen length on chromosome II are tightly linked to QTLs for petal color and volatile emission. Linkage of multiple traits will enable major phenotypic change within a few generations in hybridizing populations. Thus, the genomic architecture of pollination syndromes in Petunia allows for rapid responses to changing pollinator availability.

A novel allele of FILAMENTOUS FLOWER reveals new insights on the link between inflorescence and floral meristem organization and flower morphogenesis

Background The Arabidopsis FILAMENTOUS FLOWER (FIL) gene encodes a YABBY (YAB) family putative transcription factor that has been implicated in specifying abaxial cell identities and thus regulating organ polarity of lateral organs. In contrast to double mutants of fil and other YAB genes, fil single mutants display mainly floral and inflorescence morphological defects that do not reflect merely a loss of abaxial identity. Recently, FIL and other YABs have been shown to regulate meristem organization in a non-cell-autonomous manner. In a screen for new mutations affecting floral organ morphology and development, we have identified a novel allele of FIL, fil-9 and characterized its floral and meristem phenotypes. Results The fil-9 mutation results in highly variable disruptions in floral organ numbers and size, partial homeotic transformations, and in defective inflorescence organization. Examination of meristems indicates that both fil-9 inflorescence and floral meristems are enlarged as a result of an increase in cell number, and deformed. Furthermore, primordia emergence from these meristems is disrupted such that several primordia arise simultaneously instead of sequentially. Many of the organs produced by the inflorescence meristems are filamentous, yet they are not considered by the plant as flowers. The severity of both floral organs and meristem phenotypes is increased acropetally and in higher growth temperature. Conclusions Detailed analysis following the development of fil-9 inflorescence and flowers throughout flower development enabled the drawing of a causal link between multiple traits of fil-9 phenotypes. The study reinforces the suggested role of FIL in meristem organization. The loss of spatial and temporal organization of fil-9 inflorescence and floral meristems presumably leads to disrupted cell allocation to developing floral organs and to a blurring of organ whorl boundaries. This disruption is reflected in morphological and organ identity aberrations of fil-9 floral organs and in the production of filamentous organs that are not perceived as flowers. Here, we show the role of FIL in reproductive meristem development and emphasize the potential of using fil mutants to study mersitem organization and the related effects on flower morphogenesis.

Asymmetric Effects of Loss and Gain of a Floral Trait on Pollinator Preference

Shifts in pollination syndromes involve coordinated changes in multiple floral traits. This raises the question of how plants can cope with rapid changes in pollinator availability by the slow process of accumulation of mutations in multiple genes. Here we study the transition from bee to hawkmoth pollination in the genus Petunia. Interspecific crosses followed by single locus introgressions were used to recreate putative intermediate evolutionary stages in the evolution of moth pollination. The effect of the loss/gain of petal color was asymmetric: it had no influence on the established pollinator but enhanced visitation by the new pollinator. Therefore, shifts in pollination syndromes may proceed through intermediate stages of reduced specialization and consequently enhanced reproductive assurance. The loss of petal color in moth-pollinated Petunia involves null mutations in a single regulatory gene, An2. Such simple genetic changes may be sufficiently rapid and frequent to ensure survival during pollinator failure.

Geographic variation in floral allometry suggests repeated transitions between selfing and outcrossing in a mixed mating plant

• Premise of the study: Isometric and allometric scaling of a conserved floral plan could provide a parsimonious mechanism for rapid and reversible transitions between breeding systems. This scaling may occur during transitions between predominant autogamy and xenogamy, contributing to the maintenance of a stable mixed mating system. • Methods: We compared nine disjunct populations of the polytypic, mixed mating species Oenothera flava (Onagraceae) to two parapatric relatives, the obligately xenogamous species O. acutissima and the mixed mating species O. triloba. We compared floral morphology of all taxa using principal component analysis (PCA) and developmental trajectories of floral organs using ANCOVA homogeneity of slopes. • Key results: The PCA revealed both isometric and allometric scaling of a conserved floral plan. Three principal components (PCs) explained 92.5% of the variation in the three species. PC1 predominantly loaded on measures of floral size and accounts for 36% of the variation. PC2 accounted for 35% of the variation, predominantly in traits that influence pollinator handling. PC3 accounted for 22% of the variation, primarily in anther–stigma distance (herkogamy). During O. flava subsp. taraxacoides development, style elongation was accelerated relative to anthers, resulting in positive herkogamy. During O. flava subsp. flava development, style elongation was decelerated, resulting in zero or negative herkogamy. Of the two populations with intermediate morphology, style elongation was accelerated in one population and decelerated in the other. • Conclusions: Isometric and allometric scaling of floral organs in North American Oenothera section Lavauxia drive variation in breeding system. Multiple developmental paths to intermediate phenotypes support the likelihood of multiple mating system transitions.