Chang, S.-M. and M. D. Rausher. 1998. Frequency-dependent pollen discounting contributes to the maintenance of a mixed mating system in the common morning glory, Ipomoea purpurea. American Naturalist 152(5): 671-683.
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
Chang, S.-M. and M. D. Rausher. 1999. The role of inbreeding depression in maintaining a mixed mating system in the common morning glory, Ipomoea purpurea. Evolution 53(5): 1366-1376.
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 by 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
Rausher, M. D. and S.-M. Chang. 1999. Stabilization of mixed-mating systems by differences in the magnitude of inbreeding depression for male and female fitness components. American Naturalist 155: 242-248.
Chang, S.- M. and R. G. Shaw. 2003. The contribution of spontaneous mutation to variation in environmental response in Arabidopsis thaliana: Responses to nutrients. Evolution 57:984-994.
Though the evolutionary importance of spontaneous mutation is evident, its contribution to the evolution of ecological specificity remains unclear, because the environmental specificity of effects of new mutations has received little empirical attention. To address this issue, we report a greenhouse assay that examines the contribution of spontaneous mutation to variation in responses of A. thaliana to the concentration of nutrients in the soil. 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 5 lines representing the founder, in high and low nutrient conditions. We examined 11 traits throughout the 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 x 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 A. thaliana in previous studies.
Chang, S.-M. , Y. Lu , and M. D. Rausher. 2005. Neutral Evolution of the Non-binding Region of the Anthocyanin Regulatory Gene Ipmyb1 in Ipomoea. Genetics (170): 1967-1978
Plant transcription factors often
contain domains that evolve very rapidly. Although it has been suggested that
this rapid evolution may contribute substantially to phenotypic differentiation
among species, this suggestion has seldom been tested explicitly. We tested the
validity of this hypothesis by examining the rapidly evolving non-DNA-binding
region of an R2R3-myb transcription factor that regulates anthocyanin expression in flowers of the genus Ipomoea.
We first provide evidence that the W locus in I. purpurea,
which determines whether flowers will be pigmented or white, corresponds to a
myb gene segregating in southeastern
Chang, S.-M. 2006. Female compensation through the quantity and quality of progeny in a gynodioecious plant, Geranium maculatum (Geraniaceae) American Journal of Botany: 93: 263-270
One of the major evolutionary trends in flowering plants is the evolution of unisexual flowers (male or female) from perfect flowers. This transition has occurred repeatedly in many taxa and has generated a wonderful array of variation in sexual expression among species. Theoretical studies have proposed a number of mechanisms to explain how this level of variation could be maintained in natural systems. One possible mechanism is the female compensation hypothesis, which predicts that female mutants require an increase in their seed fitness in order to invade a hermaphroditic system. Using Geranium maculatum, I tested this hypothesis and showed that female mothers produced more and larger seeds than hermaphroditic mothers even though they were indistinguishable in their vegetative traits and the flower production. Seeds from females were also more likely to germinate and produced seedlings with larger above- and belowground biomass. These seedlings were more likely to flower than those from hermaphrodites in at least one of the two populations studied. Combined, these results indicated that females in G. maculatum did compensate for their loss of male function by producing more and better seeds than hermaphrodites. This provides a mechanism for the maintenance of female plants in this species.
Shaw, R. G. and S.-M. Chang. 2006. Gene action of new mutations in Arabidopsis thaliana. Genetics. 172: 1855-1865.
For a newly arising mutation affecting a trait under selection, its degree of dominance relative to the pre-existing 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 1 line, and fitness-reducing effects, one additive, 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.
Young, S. A., S.-M. Chang and R. R. Sharitz. 2007. Reproductive Ecology of a Federally Endangered Legume, Baptisia arachnifera, and its More Widespread Congener, Baptisia lanceolata (Fabaceae). American Journal of Botany 94(2) 228-236.
Comparisons between rare species and their more common congener species can provide valuable information for conservation. Reproductive traits have previously been shown to be critical for reproductive success and persistence of rare species. In this study, we compared floral, seedpod and seed traits of two Baptisia species (one endangered and one common) to assess differences in reproduction between species and among populations. Since heat can trigger germination in hard-seeded legumes, we also exposed Baptisia seeds to a range of high temperatures (60 ~ 100 °C) and determined seed viability. The rare B. arachnifera had significantly greater pod damage by insects and produced significantly fewer, yet heavier, seeds than B. lanceolata. While B. arachnifera seeds were not viable at temperatures above 80 °C, approximately 40% of B. lanceolata seeds maintained viability up to 100 °C. Our various seed trait measurements suggest that B. arachnifera may be a poorer colonizer than the more widespread B. lanceolata. Additionally, B. arachnifera’s reduced tolerance for high temperatures may have implications for appropriate fire management regimes for this endangered species.
Chang, S.-M. 2007. Gender specific inbreeding depression in a gynodioecious plant, Geranium maculatum (Geraniaceae). American Journal of Botany 94(7): 1193-1204.
In gynodioecious species, females coexist with hermaphrodites in natural populations even though hermaphrodites attract more pollinators, are capable of reproducing through pollen, and can self-fertilize. This study tests the hypothesis that inbreeding depression helps to maintain females in natural populations. It also examines whether gender lineages that differ in selfing rates might experience different levels of inbreeding depression. Female and hermaphroditic lineages of the gynodioecious species Geranium maculatum were used in self, sib-cross and outcross experiments to examine inbreeding depression levels and to determine whether these levels differ between hermaphroditic and female lineages. Six fitness correlates were measured in the greenhouse and compared among pollination types and between genders. Severe inbreeding depression was found for both individual fitness traits and cumulative fitness in early life history stages. Inbreeding depression levels were slightly higher in hermaphroditic than in female lineages, but this difference was not statistically significant. Because females are unable to self pollinate and are less likely to experience inbreeding than hermaphrodites under natural conditions, these results suggest that severe inbreeding depression could confer a selective advantage for females that could help to maintain females in natural populations.
Van Etten, M. L., L. B. Prevost, A. C. Deen, B. V. Ortiz, L. A. Donovan and S.-M. Chang. 2008. Gender differences in reproductive and physiological traits in a gynodioecious species, Geranium maculatum (Geraniaceae). International Journal of Plant Sciences.169: 271-279
Plant species with separate genders often exhibit gender differences in traits related to reproductive allocation. In gynodioecious species, females often produce more seeds than hermaphrodites, leading to a higher reproductive cost. The mechanisms allowing 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 cost 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 genders. We found that females produced smaller but more flowers and more fruits than 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 nitrogen (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.
Baucom, R. S., R. Mauricio and S.-M. Chang. 2008 Glyphosate induces transient male sterility in Ipomoea purpurea. Botany 86: 587-594.
Plant death is the most common effect resulting from the application of glyphosate, the active ingredient in the herbicide Roundup (R). Individual seedlings of the morning glory, Ipomoea purpurea L.aRoth, however, have been shown to exhibit tolerance to glyphosate, surviving after what should have been a lethal dose. Those that grow and reach reproductive maturity often exhibit deformed anthers within what appear to be normally developed flowers. Ipomoea purpurea has a mixed mating system and normally has hermaphroditic flowers that are capable of both selfing and outcrossing. The deformed anthers do not produce pollen, essentially converting a hermaphroditic flower to a female. Here we describe this morphological change and investigate the reproductive consequences of anther deformation. First, there is phenotypic variation for the propensity of an individual to exhibit male sterility through deformed anthers in response to treatment, but a series of field and greenhouse studies suggest that this variation is not genetic. The male sterility is also transient; within an individual, the frequency of flowers with deformed anthers declines over time. Although flowers with deformed anthers do not produce pollen, we observed mixed effects on female function of such flowers. In the greenhouse, flowers with deformed anthers that were hand-pollinated produced as many seeds as flowers with normal anthers, suggesting no effect on female fertility. In the field, however, plants with a higher proportion of anther deformation set significantly fewer seeds than those untreated, suggesting either reduced female fertility, or a reproductive penalty in flowers with deformed anthers due to the inability to self pollinate. Thus, the presence of this trait could alter the selfing to outcrossing ratio in populations that are sprayed with the herbicide. Individuals that exhibited a higher proportion of anther deformation also produce fewer total flowers than untreated plants, suggesting that anther deformation is part of a suite of responses to damage by glyphosate.
J. L. Hamrick and S.-M. Chang. 2008. Identification of glacial refugia in south-eastern
Aim We examine several hypotheses emerging from biogeographic and fossil records regarding the glacial refugia of a southern thermophilic plant species. Specifically, we investigated the glacial history and post-glacial colonization of a forest understory species, Trillium cuneatum. We focused on the following questions: (i) Did T. cuneatum survive the last glacial maximum (LGM) in multiple refugia, and where were they located? Is the contemporary genetic structure congruent with fossil-record based reconstruction of refugia for mesic deciduous forests? (ii) What are the post-glacial colonization patterns into the present geographic range? (iii) What are the patterns of genetic diversity in areas where lineages meet?
Location South-eastern North America Methods We sampled 45 locations of T. cuneatum throughout its current range. We conducted phylogeographic analyses based on maternally inherited chloroplast DNA (cpDNA haplotypes) and used TCS software to reconstruct intra-specific phylogeny.
Results We detected six cpDNA haplotypes, geographically highly structured into non overlapping areas. With one exception, none of the populations had mixed haplotype composition. TCS analysis resulted in two intraspecific cpDNA lineages, with one clade subdivided further by shallower diversification.
investigation revealed that T. cuneatum survived the
LGM in multiple refugia, belonging to two (Western,
Eastern) genealogical lineages geographically structured across south-eastern
Spigler, R. and S.-M. Chang. 2008. Effects of plant abundance on reproductive success in the widespread, native biennial Sabatia angularis (Gentianaceae): spatial scale matters. J. of Ecology.96:323-333.
1. The scope of studies examining the effect of plant abundance on reproduction thus far has been restricted mainly to rare and threatened species, leaving the question open as to whether small populations of more common species are also susceptible to reproductive disadvantages. We addressed this question by examining the effects of population size, mean population density, and local neighborhood size on fruit set, seed set, and pollen load across 20 natural populations of the widespread biennial Sabatia angularis.
2. Populations ranged in size from one to an estimated 7,700 individuals and in density from 0.12 to 3.11 individuals/m2. Population density had no effect on pollen load, fruit set or seed set. Population size significantly affected fruit set across the study populations, and this relationship was non-linear. Both small and large S. angularis populations had reduced mean fruit set relative to intermediate-sized populations. Although we did not find a similar relationship for pollen load per flower, we suggest that reduced fruit set in the smallest populations may be due to pollen limitation and due to differences in the proportion of flowers visited per plant in large populations.
3. Local neighborhood size at 1m and 4m from focal study plants had significant but opposing effects on seed set. While increases in the number of neighboring conspecifics within 1m served to reduce seed set, increases beyond that distance within 4m actually increased seed set. We conclude that these effects are due to local competition at the smallest spatial scales and facilitation for pollination beyond that distance.
4. Our study confirms that reduced reproductive success in small plant populations can occur in common species as well as in rare and endangered species and supports the emerging viewpoint that increased reproductive success with population size is a general phenomenon.
5. In contrast to most studies, our study demonstrates that the effect of increased population size for plant reproduction may cease to be positive and become negative once populations become too large. Furthermore, our study highlights the importance of incorporating multiple spatial scales when examining population dynamics.
Spigler, R. and S.-M. Chang. 2009, Pollen limitation and reproduction varies with population size in experimental populations of Sabatia angularis (Gentianaceae). Botany 87: 330-338.
Individuals in large plant populations are expected to benefit from increased reproductive success relative to those in small populations because of the facilitative effects of large aggregations on pollination. As populations become small, the inability to attract sufficient numbers of pollinators can reduce reproduction via pollen limitation. This study experimentally tested whether such trends occur for the herbaceous biennial Sabatia angularis (L.) Pursh (Gentianaceae). We created artificial populations of varying size consisting of potted S. angularis plants in two field sites to determine whether population size affected mean fruit and seed set. We also examined whether population size affected the degree of pollen limitation using a supplemental pollination design in one of the sites. Our results showed that, on average, seed set was lower in large populations, not small populations, of S. angularis and that this result may be due to increased pollen limitation in large populations. We suggest that in certain contexts, small populations may enjoy reproductive advantages over large populations by escaping intraspecific competition for pollinators.
Van Etten, M. L. and S.-M. Chang. 2009. Effects of environmental heterogeneity on the distribution of genders within and among populations in a gynodioecious species, Geranium maculatum. New Phytologist 183: 649-660.
Populations containing both females and hermaphrodites (dimorphic) are generally found in drier sites than those with only hermaphrodites (monomorphic). The sex-differential plasticity hypothesis (SDP) suggests that this is caused by hermaphrodites reducing allocation to seeds in harsh environments, allowing female establishment. We proposed that a similar process could explain sex distribution within populations. We compared light availability and soil moisture between sites of three monomorphic and three dimorphic populations of Geranium maculatum and between microsites occupied by females and hermaphrodites within populations. We also correlated seed production in dimorphic populations with environmental measures. We found that dimorphic and monomorphic populations occurred in sites with similar soil moisture but within two dimorphic populations females occurred in drier microsites than hermaphrodites, as predicted by the SDP hypothesis. Contrary to the predictions, hermaphrodites' seed production was not influenced by the environment. Rather, females' seed production was correlated with environmental conditions in two populations, although the direction of the correlation differed between populations. Our results suggest that in this species, the SDP hypothesis does not explain sex distribution among or within populations. However, microsite environments may influence the distribution of sexes within a population and potentially aid in maintaining gynodioecy.
Spigler, R., J. L. Hamrick, and S.-M. Chang. 2010. Increased inbreeding but not homozygosity in small populations of Sabatia angularis (Gentianaceae). Plant Systematics and Evolution 284: 131-140.
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.
Armstrong, N.A. and S.-M. Chang. 2007. Location, Location, Location: Does seat location affect achievement in very large classes? Journal of College Science Teaching. 37(2): 54-58
Armstrong, N.A., S.-M. Chang and P. Brickman. 2007. Cooperative learning in industrial sized biology classes. CBE Life Science Education. 6: 163-171.
Armstrong, N.A., C. S. Wallace and S.-M. Chang. 2008. Learning from Writing Scientific Arguments in College Biology. Journal of Research in Science Education 38:483-499.