Shu-Mei Chang

THE ROLE OF INBREEDING DEPRESSION IN MAINTAINING THE MIXED MATING SYSTEM OF THE COMMON MORNING GLORY, IPOMOEA PURPUREA

Theoretical studies show that, although inbreeding depression (ID) will counterbalance the transmission advantage of selfing, it can only maintain a mixed mating system in plants when at least one of the following two conditions is met: (1) there is a positive association between selfing rates and the level of ID; and (2) ID is greater than 0.5 for the female component of fitness, while the average ID for male and female fitness is less than 0.5. This study tests whether these two conditions hold in the common morning glory, Ipomoea purpurea, which has a mixed mating system with 30% self‐fertilization. Inbreeding depression was found in all but one fitness component measured in two groups of plants with distinct anther‐stigma distances (ASD), a character that influences selfing rates. However, when examined separately, a negative association was found between selfing rates and ID; plants with large ASD (low‐selfing‐rate genotypes) tended to have higher ID than ones with small ASD (high‐selfing‐rate genotypes). Furthermore, the overall lifetime ID for male (12.5%) and female (24%) components of fitness, averaged across two ASD groups, were lower than what is necessary for ID to maintain an evolutionarily stable mixed mating system. Therefore, although inbreeding depression contributes to balancing the transmission advantage of selfing, it is not likely to be the primary mechanism maintaining the mixed mating system of I. purpurea. The contribution of other mechanisms is discussed.

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.

THE CONTRIBUTION OF SPONTANEOUS MUTATION TO VARIATION IN ENVIRONMENTAL RESPONSES OF ARABIDOPSIS THALIANA: RESPONSES TO LIGHT

Abstract Although the evolutionary importance of spontaneous mutation is evident, its contribution to the evolution of ecological specificity remains unclear, because the environmental sensitivity of effects of new mutations has received little empirical attention. To address this issue, we report a greenhouse in which we grew plants from 20 mutation‐accumulation (MA) lines, advanced by selfing and single‐seed descent from a single common founder to generation 17, as well as plants from five lines representing the founder, in high and low nutrient conditions. We examined 11 traits throughout life history, including germination, survivorship, bolting date, flowering date, leaf number, leaf size, early and late height, mean fruit size, total seed weight, and reproductive biomass. Comparison of trait means between the two generations did not support the commonly held view that new mutations affecting fitness in these MA lines are strongly biased toward deleterious effects. We detected significant variance among MA lines for one fitness component, mean fruit size, but we did not detect a significant contribution of mutations accumulated in these MA lines to genotype by environment interaction (GEI). These results suggest that other evolutionary mechanisms play a more important role than spontaneous mutation alone in establishing the GEI found for wild collections and lab accessions of Arabidopsis thaliana in previous studies.

Stabilization of Mixed‐Mating Systems by Differences in the Magnitude of Inbreeding Depression for Male and Female Fitness Components

Although a majority of plant species exhibit either complete selfing or complete outcrossing, a distinct minority exhibit a mixed-mating system, in which both selfing and outcrossing occur (Schemske and Lande 1985). Moreover, in at least some species with mixed-mating systems, selfing rates are genetically variable (Brown and Clegg 1984; Holtsford and Ellstrand 1992; Carr and Fenster 1994; Chang and Rausher 1998), suggesting that these mixedmating systems are evolutionarily stable. Theoretical attempts to account for such stability have generally focused on assessing the conditions under which two opposing sets of evolutionary processes can generate polymorphisms for selfing rates. One of these processes, originally described by Fisher (1941), arises because an allele that increases the selfing rate automatically enjoys a transmission advantage due to the extra pathway (via self-pollenation) by which it may transmit copies of itself to the next generation. Various authors have demonstrated that, under some circumstances, two other processes—inbreeding depression and pollen discounting—may prevent fixation of such a selfing allele and stabilize a selfing-rate polymorphism (Holsinger 1988, 1991; Charlesworth and Charlesworth 1990; Uyenoyama and Waller 1991b). In particular, under some circumstances the identity disequilibrium that is expected to arise between loci affecting selfing rate and loci affecting fitness through inbreeding depression may be strong enough to stabilize polymorphisms at both sets of

Gender Differences in Reproductive and Physiological Traits in a Gynodioecious Species, Geranium maculatum (Geraniaceae)

Plant species with separate genders often exhibit gender differences in traits related to reproductive allocation. In gynodioecious species, females often produce more seeds than do hermaphrodites, leading to a higher reproductive cost. The mechanisms that allow females to meet the high costs of reproduction are currently under debate. In this study, we test the hypothesis that there are genetically based gender differences in physiological traits that enable females to finance these costs through higher photosynthetic carbon gain in the gynodioecious perennial Geranium maculatum. Females and hermaphrodites were compared in a greenhouse study that minimized environmental and selfing rate differences between the genders. We found that females produced smaller flowers but more of them and more fruits than did hermaphrodites. However, genders did not differ in their seed number, seed mass, fruit set, and reproductive allocation. In addition, genders did not differ in photosynthetic rate (A), leaf N, and water use efficiency inferred from leaf carbon isotope ratio (δ13C). Overall, G. maculatum shows no genetically based gender differences for most of the reproductive traits or any of the physiological traits measured. Our results suggest that for G. maculatum, the gender fitness differences previously identified in natural populations may be caused by gender differences in microhabitat and/or selfing rate.

The geographic mosaic of herbicide resistance evolution in the common morning glory, Ipomoea purpurea: Evidence for resistance hotspots and low genetic differentiation across the landscape

Strong human‐mediated selection via herbicide application in agroecosystems has repeatedly led to the evolution of resistance in weedy plants. Although resistance can occur among separate populations of a species across the landscape, the spatial scale of resistance in many weeds is often left unexamined. We assessed the potential that resistance to the herbicide glyphosate in the agricultural weed Ipomoea purpurea has evolved independently multiple times across its North American range. We examined both adaptive and neutral genetic variations in 44 populations of I. purpurea by pairing a replicated dose–response greenhouse experiment with SSR genotyping of experimental individuals. We uncovered a mosaic pattern of resistance across the landscape, with some populations exhibiting high‐survival postherbicide and other populations showing high death. SSR genotyping revealed little evidence of isolation by distance and very little neutral genetic structure associated with geography. An approximate Bayesian computation (ABC) analysis uncovered evidence for migration and admixture among populations before the widespread use of glyphosate rather than the very recent contemporary gene flow. The pattern of adaptive and neutral genetic variations indicates that resistance in this mixed‐mating weed species appears to have evolved in independent hotspots rather than through transmission of resistance alleles across the landscape.

Inbreeding depression in male gametic performance

One key objective in evolutionary ecology is to understand the magnitude of inbreeding depression expressed across sex‐specific components of fitness. One major component of male fitness is fertilization success, which depends on male gametic performance (sperm and pollen performance in animals and plants, respectively). Inbreeding depression in male gametic performance could create sex‐specific inbreeding depression in fitness, increase the benefit of inbreeding avoidance and reduce the efficacy of artificial insemination and pollination. However, there has been no assessment of the degree to which inbreeding generally depresses male gametic performance and hence post‐copulatory or post‐pollination fertilization success. Because inbreeding depression is understood to be a property of diploid entities, it is not clear what degree of inbreeding depression in haploid gametic performance should be expected. Here, we first summarize how inbreeding depression in male gametic performance could potentially arise through gene expression in associated diploid cells and/or reduced genetic diversity among haploid gametes. We then review published studies that estimate the magnitude of inbreeding depression in traits measuring components of sperm or pollen quantity, quality and competitiveness. Across 51 published studies covering 183 study traits, the grand mean inbreeding load was approximately one haploid lethal equivalent, suggesting that inbreeding depresses male gametic performance across diverse systems and traits. However, there was an almost complete lack of explicit estimates from wild populations. Future studies should quantify inbreeding depression in systematic sets of gametic traits under naturally competitive and noncompetitive conditions and quantify the degree to which gamete phenotypes and performance reflect haploid vs. diploid gene expression.

Increased inbreeding but not homozygosity in small populations of Sabatia angularis (Gentianaceae).

Understanding how the mating system varies with population size in plant populations is critical for understanding their genetic and demographic fates. We examined how the mating system, characterized by outcrossing rate, biparental inbreeding rate, and inbreeding coefficient, and genetic diversity varied with population size in natural populations of the biennial Sabatia angularis. We found a significant, positive relationship between outcrossing and population size. Selfing was as high as 40% in one small population but was only 7% in the largest population. Despite this pattern, observed heterozygosity did not vary with population size, and we suggest that selection against inbred individuals maintains observed heterozygosity in small populations. Consistent with this hypothesis, we found a trend of lower inbreeding coefficients in the maternal than progeny generation in all of the populations, and half of the populations exhibited significant excesses of adult heterozygosity. Moreover, genetic diversity was not related to population size and was similar across all populations examined. Our results suggest that the consequences of increased selfing for population fitness in S. angularis, a species that experiences significant inbreeding depression, will depend on the relative magnitude and consistency of inbreeding depression and the demographic cost of selection for outcrossed progeny in small populations.

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.

Gene Action of New Mutations in Arabidopsis thaliana

For a newly arising mutation affecting a trait under selection, its degree of dominance relative to the preexisting allele(s) strongly influences its evolutionary impact. We have estimated dominance parameters for spontaneous mutations in a subset of lines derived from a highly inbred founder of Arabidopsis thaliana by at least 17 generations of mutation accumulation (MA). The labor-intensive nature of the crosses and the anticipated subtlety of effects limited the number of MA lines included in this study to 8. Each MA line was selfed and reciprocally crossed to plants representing the founder genotype, and progeny were assayed in the greenhouse. Significant mutational effects on reproductive fitness included a recessive fitness-enhancing effect in one line and fitness-reducing effects, one additive and the other slightly recessive. Mutations conferring earlier phenology or smaller leaves were significantly recessive. For effects increasing leaf number and reducing height at flowering, additive gene action accounted for the expression of the traits. The sole example of a significantly dominant mutational effect delayed phenology. Our findings of recessive action of a fitness-enhancing mutational effect and additive action of a deleterious effect counter a common expectation of (partial) dominance of alleles that increase fitness, but the frequency of occurrence of such mutations is unknown.