The evolutionary potential of Baker's weediness traits in the common morning glory, Ipomoea purpurea (Convolvulaceae)

? Premise of the study: Many reports have cited Baker's list of weediness traits, or those that exemplify the "ideal" weed, yet few have considered the evolutionary potential of such traits as a group. Thus, it is unknown whether constraints on the evolution of increased weediness, such as a lack of genetic variation or genetic correlations between the traits, are present. Ipomoea purpurea, the common morning glory, is a problematic weed that exhibits many of Baker's ideal weed traits. ? Methods: We used progeny from a half/full-sib breeding design in a series of three greenhouse experiments to assess the presence of genetic variation, narrow sense heritabilities, and genetic correlations in Baker's growth, competition, and fitness "weediness" traits in two populations of I. purpurea. ? Key results: We uncovered genetic variation underlying reproductive fitness traits and competitive ability in at least one population, but no evidence of genetic variation underlying growth rate in either population. Genetic correlations between many of the weediness characters differed significantly from zero; however, their direction and/or magnitude differed between populations. ? Conclusions: We found that increased weediness in the common morning glory is more likely to occur through selection on reproductive output and competitive ability rather than through selection on growth rate. Assessing Baker's traits in a quantitative genetics framework can provide a solid perspective on their evolutionary potential and a unique framework within which to determine how weeds will respond to different environmental stresses and/or scenarios of global climate change.     

Natural selection on two seed-size traits in the common morning glory Ipomoea purpurea (Convolvulaceae): patterns and evolutionary consequences

Plants may express two separate seed-size characters during their lifetimes: the size of the seeds from which they germinate (initial seed size) and the mean size of seed they produce as adults (maternal seed size). Many empirical studies indicate that selection often favors a larger initial seed size. In contrast, patterns of natural selection on maternal seed size have not been measured, although theory often predicts stabilizing selection. Here, I report on a field study of the common morning glory Ipomoea purpurea, which provided measurements of natural selection on both initial and maternal seed size. For initial seed size, selection favored larger seeds, but a greenhouse study indicated no genetic variation for this trait. For maternal seed size, there was no evidence of either directional or stabilizing selection, but there was significant additive genetic variation. The genetic correlation between the number and size of seeds was not significant, indicating no trade-off between these traits, but a negative genetic correlation was found between maternal seed size and the probability of surviving to reproduce. The absence of the predicted pattern of stabilizing selection on maternal seed size in the study population highlights the need for more empirical work on the evolution of seed size.     

Frequency-dependent pollen discounting contributes to maintenance of a mixed mating system in the common morning glory Ipomoea purpurea

Pollen discounting, a reduction in outcross success associated with increased selfing, was evaluated in the common morning glory Ipomoea purpurea. A field experiment was conducted to estimate selfing rates and outcross success using small arrays of plants with large or small anther-stigma distance (ASD). To evaluate the effect of genotypic composition on the mating-system parameters, arrays were composed of five different frequencies of small- and large-ASD genotypes. While the selfing rates of genotypes with small ASD were consistently higher than genotypes with large ASD regardless of the genotypic frequency, outcross success was negatively frequency dependent. The genotype that was at lower frequency in the array had higher outcrossing success in three out of the four array types with unequal frequencies. This advantage-when-rare phenomenon can contribute to preventing the fixation of either extreme ASD-morph and maintaining a mixed mating system in I. purpurea.     

Nucleotide polymorphism in the chalcone synthase-A locus and evolution of the chalcone synthase multigene family of common morning glory Ipomoea purpurea

Chalcone synthase (CHS) is a small multigene family with at least four members (CHS-A, B, C and PS) in common morning glory Ipomoea purpurea ROTH. The chalcone synthase enzyme performs the initial condensation reaction that results in the 15-carbon three-ring structure that is the backbone of flavonoid biosynthesis. The biochemical pathway that commences with CHS is important in plant disease defence, pigment biosynthesis and UV protection. Accordingly, it is of substantial interest to characterize levels and patterns of molecular diversity for genes that encode this important enzyme. We report the sequence of 19 CHS-A alleles from Mexican and American populations of common morning glory. American populations of this annual self-compatible vine are believed to have been introduced from Mexico, where the species is native. Individual plants were sampled from populations of common morning glory throughout Mexico and the south-eastern USA. Four American alleles were sequenced and these, together with one allele from Mexico City, were identical in primary nucleotide sequence. These data suggest a restricted origin for the American population, probably as a consequence of selection for domestication by pre-Columbian peoples. Additionally the Mitontic (Chiapas, Mexico) population is significantly more homogeneous than expected by chance indicating that this population may also have experienced a recent population bottleneck. Estimates of nucleotide diversity from the Mexican CHS-A alleles were high. We present evidence that these estimates may, in part, result from low to moderate levels of interlocus recombination/gene conversion. We also present evidence that the ancient duplication of the CHS gene family, preceding the origin of the genus Ipomoea, was associated with heterogeneity in the rate of substitution between the resulting gene family members. The group of gene family members whose sequences possess a signature amino acid of the closely related Stilbene synthase exhibit a significantly faster proportional rate of nonsynonymous substitution.     

Effect of water availability on tolerance of leaf damage in tall morning glory,Ipomoea purpurea

Resource availability may limit plant tolerance of herbivory. To predict the effect of differential resource availability on plant tolerance, the limiting resource model (LRM) considers which resource limits plant fitness and which resource is mostly affected by herbivore damage. We tested the effect of experimental drought on tolerance of leaf damage in Ipomoea purpurea, which is naturally exposed to both leaf damage and summer drought. To seek mechanistic explanations, we also measured several morphological, allocation and gas exchange traits. In this case, LRM predicts that tolerance would be the same in both water treatments. Plants were assigned to a combination of two water treatments (control and low water) and two damage treatments (50% defoliation and undamaged). Plants showed tolerance of leaf damage, i.e., a similar number of fruits were produced by damaged and undamaged plants, only in control water. Whereas experimental drought affected all plant traits, leaf damage caused plants to show a greater leaf trichome density and reduced shoot biomass, but only in low water. It is suggested that the reduced fitness (number of fruits) of damaged plants in low water was mediated by the differential reduction of shoot biomass, because the number of fruits per shoot biomass was similar in damaged and undamaged plants. Alternative but less likely explanations include the opposing direction of functional responses to drought and defoliation, and resource costs of the damage-induced leaf trichome density. Our results somewhat challenge the LRM predictions, but further research including field experiments is needed to validate some of the preliminary conclusions drawn.     

Experimental evidence that selection favors character displacement in the ivyleaf morning glory

While there is abundant evidence to suggest that pollinators influence the evolution of plant floral traits, there is little direct evidence that interactions between plant species shape the evolution of such characteristics. The purpose of this study was to determine whether the presence of the morning glory Ipomoea purpurea alters patterns of selection on floral traits of its congener, Ipomoea hederacea. We show that while selection on I. hederacea floral traits is effectively neutral when I. purpurea flowers are absent, selection acts to increase clustering of anthers about the stigma when I. purpurea flowers are present. Our results provide direct experimental evidence that the presence of flowers of a co-occurring congener can influence patterns of natural selection on floral traits that influence the mating system and contribute to prezygotic isolation. To the extent that this result is general, it also lends support to the claim that distributional patterns interpreted as ecological and reproductive character displacement in other plant species have been caused by natural selection generated by interactions among plant species.     

Pollinator response to male floral display size in two Sagittaria (Alismataceae) species

One hypothesis for the evolution of maleness in plants postulates the following: male plants appear that have re-allocated resources from female parts into a larger number of male flowers, creating a larger floral display. Pollinators respond “dramatically” to the increased display, driving the spread of males in the population (Bawa, K. S., 1980, Annual Review of Ecology and Systematics 11:15–40). To test this, we measured the total number of flowers and the size of male displays in dioecious Sagittaria latifolia and monoecious S. australis. We also measured how fast visitors arrived at “target” flowers in the displays. Then we used the Cox Model, a failure time analysis procedure, to analyze the relationship between visitor arrival and display size. We found that male display sizes were somewhat larger in the dioecious than the monoecious plants, but this was due to more compressed blooming rather than to a larger total number of flowers. The visitors to both plants were similar arrays of generalist bees. Visitors did not show the predicted “dramatic” response, however, but rather a plateauing response to larger display sizes, so our results do not support the hypothesis. Reviewing the literature, we found no reports of the “dramatic” response the hypothesis asserts. Instead, relative insensitivity to display size is the rule.     

Phenotypic responses of the twining vine Ipomoea purpurea (Convolvulaceae) to physical support availability in sun and shade

Vines depend on external support to prevent shading by neighbouringplants. Hence, it is important to determine whether shading enhances thephenotypic responses of vines to support availability. I evaluated theconsequences of support availability (a vertical stake) on shoot and leaftraitsof the morning glory Ipomoea purpurea (Convolvulaceae)under full sunlight and extreme shade. It was hypothesised that phenotypicresponses of vines to support availability should be greater in the shade. Inaddition, to investigate possible constraints to such phenotypic responses, thecorrelations among phenotypic traits and the plasticity of such correlationswere evaluated. The phenotypic variation of the main stem length and of thenumber of branches was consistent with the hypothesis, i.e. greater responsestosupport availability in the shade. In contrast, both internode length and leafarea (two traits that showed a significant and positive correlation) decreasedin the sun and increased in the shade with support availability. Petiole lengthdecreased with support in the sun but had no response in the shade. On theotherhand, the number of significant trait correlations found in plants in the sunand supported plants was higher than those of shade and non-supported plants,respectively. Several of the correlations were significantly sensitive to theenvironment. Flowering only occurred in the sun treatment. Whereas no shoot orleaf trait was significantly correlated with flower number in supported plants,both petiole length and shoot biomass showed a significant correlation withsuchestimate of plant fitness in non-supported plants.     

Genetics of resistance to the rust fungus Coleosporium ipomoeae in three species of morning glory (Ipomoea)

We examined the genetic basis of resistance to the rust pathogen Coleosporium ipomoea in three host species: Ipomoea purpurea, I. hederacea, and I. coccinea (Convolvulaceae). In crosses between resistant and susceptible individuals, second-generation selfed offspring segregated in ratios that did not differ statistically from the 3:1 ratio indicative of single-gene resistance with the resistant allele dominant. One out of three crosses between resistant individuals from two different populations revealed that resistance loci differed in the two populations, as evidenced by the production of susceptible individuals among the S(2) generation. These results suggest that gene-for-gene interactions contribute substantially to the dynamics of coevolution in this natural pathosystem. They also suggest that evolution of resistance to the same pathogen strain may involve different loci in different Ipomoea populations.     

Nuclear fragmentation and DNA degradation during programmed cell death in petals of morning glory (Ipomoea nil)

We studied DNA degradation and nuclear fragmentation during programmed cell death (PCD) in petals of Ipomoea nil (L.) Roth flowers. The DNA degradation, as observed on agarose gels, showed a large increase. Using DAPI, which stains DNA, and flow cytometry for DAPI fluorescence, we found that the number of DNA masses per petal at least doubled. This indicated chromatin fragmentation, either inside or outside the nucleus. Staining with the cationic lipophilic fluoroprobe DiOC₆ indicated that each DNA mass had an external membrane. Fluorescence microscopy of the nuclei and DNA masses revealed an initial decrease in diameter together with chromatin condensation. The diameters of these condensed nuclei were about 70% of original. Two populations of nuclear diameter, one with an average diameter about half of the other, were observed at initial stages of nuclear fragmentation. The diameter of the DNA masses then gradually decreased further. The smallest observed DNA masses had a diameter less than 10% of that of the original nucleus. Cycloheximide treatment arrested the cytometrically determined changes in DNA fluorescence, indicating protein synthesis requirement. Ethylene inhibitors (AVG and 1-MCP) had no effect on the cytometrically determined DNA changes, suggesting that these processes are not controlled by endogenous ethylene.     

Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomoea hederacea

Recent work defines coevolution between plants and herbivores as pairwise when the pattern of selection on resistance traits and the response to selection are both independent of the presence or absence of other herbivores. In addition, for a pairwise response to selection, resistance to a focal herbivore must have the same genetic basis in the presence and absence of other herbivores. None of these conditions were satisfied for the ivyleaf morning glory, Ipomoea hederacea, and its insect, fungal, and mammalian natural enemies with a quantitative genetics field experiment. A significant negative genetic correlation exists between resistance to deer and generalist insect herbivory that would preclude an independent response to selection. In addition, resistance loci under selection differ depending on the composition of the natural enemy community as indicated by genetic correlations between deer resistances in the presence and absence of other natural enemies that differ substantially from 1. Finally, selection on deer resistance depends on the presence or absence of insects; in the presence of insects, greater deer resistance is favored, but in the absence of insects, deer resistance is effectively neutral. These results indicate that the composition of the natural enemy community can alter both the pattern of selection and the likely response to selection of resistance traits.     

Effects of floral display size on male and female reproductive success in Mimulus ringens

Background and Aims

The number of flowers blooming simultaneously on a plant may have profound consequences for reproductive success. Large floral displays often attract more pollinator visits, increasing outcross pollen receipt. However, pollinators frequently probe more flowers in sequence on large displays, potentially increasing self-pollination and reducing pollen export per flower. To better understand how floral display size influences male and female fitness, we manipulated display phenotypes and then used paternity analysis to quantify siring success and selfing rates.

Methods

To facilitate unambiguous assignment of paternity, we established four replicate (cloned) arrays of Mimulus ringens, each consisting of genets with unique combinations of homozygous marker genotypes. In each array, we trimmed displays to two, four, eight or 16 flowers. When fruits ripened, we counted the number of seeds per fruit and assigned paternity to 1935 progeny.

Key Results

Siring success per flower declined sharply with increasing display size, while female success per flower did not vary with display. The rate of self-fertilization increased for large floral displays, but siring losses due to geitonogamous pollen discounting were much greater than siring gains through increased self-fertilization. As display size increased, each additional seed sired through geitonogamous self-pollination was associated with a loss of 9·7 seeds sired through outcrossing.

Conclusions

Although total fitness increased with floral display size, the marginal return on each additional flower declined steadily as display size increased. Therefore, a plant could maximize fitness by producing small displays over a long flowering period, rather than large displays over a brief flowering period.     

Temporal variation in floral display size and individual floral sex allocation in racemes of Narthecium asiaticum (Liliaceae)

We analyzed the effects of temporal variation in floral display size (number of flowers open at one time on a plant) on the rate of pollen removed and receipt of individual flowers for the sequential blooming plant Narthecium asiaticum (Liliaceae). Because of the acropetal blooming of this species, the display sizes when upper flowers opened was much greater than the display sizes when lower flowers opened. Our experiments revealed that large displays lead to a high rate of pollen removal from individual flowers, though they do not lead to a high rate of ovule fertilization. Consequently, the rate of pollen grains removed per flower by pollinators was greater in upper flowers than in lower flowers. The pattern of sex allocation in individual flowers within a raceme was consistent with such variation. Namely, both maleness [stamen mass/(stamen mass + pistil mass)] and pollen?:?ovule ratio were larger in upper flowers. We suggest that the temporal variation in display size, in addition to such factors as dichogamy and pollinator directionality, also produces variation in the probability of successful pollen transfer from individual flowers that may cause the variation in the sex allocation of individual flowers.     

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. Second affiliation for Mark Van Kleunen is temporary until February 2007.