Morning glory as a powerful model in ecological genomics: tracing adaptation through both natural and artificial selection.

Many diverse questions in ecology and evolution have been addressed using species belonging to the genus Ipomoea, commonly referred to as the morning glory genus. Ipomoea exhibits a wide range of diversity in floral color, growth form, mating system and tolerance to environmental factors, both within and among species, and as such has been a focal group of many investigations in the last 80 years. In this review, we highlight recent work to which Ipomoea species have contributed-from studies of the mating system, molecular evolution, plant-herbivore and plant-parasite interactions to their impact on and importance to agriculture. Genomic resources for this group are currently under development, and given the breadth of studies and history of this group, combined with an expanding genetics toolkit, we argue that Ipomoea should provide the next model organism for ecological genomics.

Search image for leaf shape in a butterfly.

The butterfly Battus philenor forms search images for leaf shape when searching for its two larval host plants in southeast Texas. This behavior increases the rate of discovery of host plants and permits females to track changes in relative host plant suitability for larval growth. Apostatic selection resulting from search image formation is a likely explanation for divergence in leaf shape by the two host plants.

Genetic analysis of coevolution between plants and their natural enemies.

Plants exhibit a diverse array of characteristics that have been interpreted as functioning primarily as defenses against natural enemies, such as pathogens and herbivores. Recent genetic analyses of resistance provide evidence supporting this interpretation. In addition, these analyses also support a key assumption underlying models of the evolution of resistance (i.e. that resistance is costly) and suggest that the outcome of coevolution is often not explainable in terms of pairwise interactions between a plant and individual natural enemies (i.e. coevolution is often likely to be diffuse rather than pairwise).

Effects of a locus affecting floral pigmentation in Ipomoea purpurea on female fitness components.

A locus influencing floral pigment intensity in the morning glory, Ipomoea purpurea, is polymorphic throughout the southeastern United States. Previous work has suggested that the white allele at this locus has a transmission advantage during mating because of the effect of flower color on pollinator behavior. The experiment described here was designed to determine whether other effects of the W locus may contribute an opposing selective advantage to the dark allele. Dark homozygotes were vegetatively smaller and produced fewer flowers, seed capsules and seeds than either light heterozygotes or white homozygotes. In addition, dark homozygotes produced smaller seeds than heterozygotes, and there is some indication that white homozygotes also produced smaller seeds than heterozygotes. Pleiotropic effects on seed number thus do not seem to contribute to selection opposing the mating advantage associated with the white allele. However, pleiotropic effects on seed size might contribute to overdominance that could stabilize the W locus polymorphism.

Balancing selection on a floral polymorphism.

The common morning glory, Ipomoea purpurea, exhibits a flower color polymorphism at the W locus throughout the southeastern North America. The W locus controls whether flowers will be darkly pigmented (WW), lightly pigmented (Ww), or white with pigmented rays (ww). In this report, we describe results of a perturbation, or convergence, experiment using five plots designed to determine whether balancing selection operates on the W locus. The pattern of gene frequency changes obtained are indicative of balancing selection operating at the W locus, providing direct evidence that both the alleles are actively maintained by selection.

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.

Genetic differences and phenotypic plasticity as causes of variation in oviposition preference in Battus philenor.

Bradshaw (1965) proposed that phenotypic plasticity would be more common than adaptive genetic variability in species for which environmental fluctuations occur over periods roughly equal to that species' generation time. In an effort to examine this notion, sources of seasonal variation in two components of oviposition behavior in an east Texas population of pipevine swallowtail butterflies (Battus philenor) were investigated under natural and seminatural conditions. Variability in a visually-based prealighting component involving orientation to leaf shape was primarily due to phenotypic plasticity in the form of adult learning; no seasonally-based genotypic differences in leaf-shape discrimination behavior were observed. By contrast, a chemotactile post-alighting component involving elicitation of oviposition after landing on the host plant was not phenotypically plastic, i.e., not susceptible to learning. In addition, only slight and nonsignificant seasonally-based differences in post-alighting responses to different host species were observed.

Co-evolution and plant resistance to natural enemies.

Co-evolution between plants and their natural enemies is generally believed to have generated much of the Earth's biological diversity. A process analogous to co-evolution occurs in agricultural systems, in which natural enemies adapt to crop resistance introduced by breeding or genetic engineering. Because of this similarity, the investigation of resistance mechanisms in crops is helping to elucidate the workings of co-evolution in nature, while evolutionary principles, including those derived from investigation of co-evolution in nature, are being applied in the management of resistance in genetically engineered crops.

Floral-color polymorphism in Ipomoea purpurea: biased inheritance of the dark allele is not a general explanation for its maintenance.

A previous investigation reported the existence in a single population of the morning glory (Ipomoea purpurea) of non-Mendelian inheritance at the W locus influencing flower color. In addition, it was shown that the magnitude of biased inheritance in that population was sufficient to maintain a floral-color polymorphism at that locus at frequencies approximating those observed in natural populations. The current investigation was undertaken to determine whether this biased inheritance was characteristic of other I. purpurea populations, and thus whether it provides a general explanation for maintenance of the polymorphism. The current study found no evidence for biased inheritance in two additional polymorphic populations examined. Non-Mendelian inheritance thus seems unlikely to constitute a general explanation for the maintenance of this floral-color polymorphism in l. purpurea.

The genetic basis of a flower color polymorphism in the common morning glory (Ipomoea purpurea).

The common morning glory (Ipomoea purpurea) is highly polymorphic for flower color. Part of this phenotypic variation is due to allelic variation at the P locus. This locus determines whether flowers will be purple or pink, where purple is dominant to pink. We have determined that the anthocyanin biosynthetic gene flavonoid 3'-hydroxylase (f3'h) corresponds to the P locus. In the pink allele of f3'h there is a large insertion in the third exon, which results in the production of a truncated transcript. This shortened transcript produces a nonfunctional F3'H enzyme, resulting in the production of pink flowers rather than purple. In addition, we describe a polymerase chain reaction (PCR)-based assay that can be used to determine the genotype of a plant at this locus.

Analysis of a chalcone synthase mutant in Ipomoea purpurea reveals a novel function for flavonoids: amelioration of heat stress.

Flavonoids are thought to function in the plant stress response and male fertility in some, but not all, species. We examined the effects of a self-fertile chalcone synthase null allele, a, for the effects of heat and light stress on fertilization success and flower production in Ipomoea purpurea. Pollen recipients and pollen donors of both homozygous genotypes exhibit reduced fertilization success at high temperatures, indicating that high temperature acts as a stress-lowering fertilization success. Homozygous aa individuals exhibit reduced male and female fertilization success, compared to AA individuals, at high temperatures but not at low temperatures. In addition, aa individuals produce fewer flowers than AA individuals at low temperatures, but not at high temperatures. These results suggest that flavonoids alleviate heat stress on fertilization success. They also suggest that pleiotropic effects at the A locus may explain the low frequency of the a allele in natural populations.

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.

Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway.

The anthocyanin biosynthetic pathway is responsible for the production of anthocyanin pigments in plant tissues and shares a number of enzymes with other biochemical pathways. The six core structural genes of this pathway have been cloned and characterized in two taxonomically diverse plant species (maize and snapdragon). We have recently cloned these genes for a third species, the common morning glory, Ipomoea purpurea. This additional information provides an opportunity to examine patterns of evolution among genes within a single biochemical pathway. We report here that upstream genes in the anthocyanin pathway have evolved substantially more slowly than downstream genes and suggest that this difference in evolutionary rates may be explained by upstream genes being more constrained because they participate in several different biochemical pathways. In addition, regulatory genes associated with the anthocyanin pathway tend to evolve more rapidly than the structural genes they regulate, suggesting that adaptive evolution of flower color may be mediated more by regulatory than by structural genes. Finally, for individual anthocyanin genes, we found an absence of rate heterogeneity among three major angiosperm lineages. This rate constancy contrasts with an accelerated rate of evolution of three CHS-like genes in the Ipomoea lineage, indicating that these three genes have diverged without coordinated adjustment by other pathway genes.