Johanna Schmitt

Testing the Adaptive Plasticity Hypothesis: Density-Dependent Selection on Manipulated Stem Length in Impatiens capensis

In plants, stem elongation at high density in response to vegetation shade is hypothesized to be an example of adaptive phenotypic plasticity. Elongated stems may increase the light capture for plants in dense stands, while nonelongated stems may be favored for plants in low density. We tested the adaptive value of plastic stem elongation in Impatiens capensis by manipulating the controlling light cue, red to far red ratio, to produce elongated and nonelongated plants. These plants were then transplanted into high and low densities in a natural population. The results supported the adaptive plasticity hypothesis; elongated plants were more fit at high density, and suppressed plants were more fit at low density. Phenotypic selection analysis revealed selection for increased height in high density and for decreased height relative to leaf length in low density. Elongated plants showed less growth of the second internode at 2 wk after transplantation in both densities, which suggests a cost of elongation. Direct selection on height explained the fitness differences between suppressed and elongated plants at high density, but it did not completely explain the lower fitness of elongated plants at low density, which implies an intrinsic cost of elongation independent of selection on morphology.

A Map of Local Adaptation in Arabidopsis thaliana

Field experiments identify loci associated with fitness and local adaptation in Arabidopsis. Local adaptation is critical for species persistence in the face of rapid environmental change, but its genetic basis is not well understood. Growing the model plant Arabidopsis thaliana in field experiments in four sites across the species’ native range, we identified candidate loci for local adaptation from a genome-wide association study of lifetime fitness in geographically diverse accessions. Fitness-associated loci exhibited both geographic and climatic signatures of local adaptation. Relative to genomic controls, high-fitness alleles were generally distributed closer to the site where they increased fitness, occupying specific and distinct climate spaces. Independent loci with different molecular functions contributed most strongly to fitness variation in each site. Independent local adaptation by distinct genetic mechanisms may facilitate a flexible evolutionary response to changing environment across a species range.

The Evolution of Plant Ecophysiological Traits: Recent Advances and Future Directions

lants exhibit enormous ecophysiological and functional diversity, which underlies variation in growth rates, productivity, population and community dynamics, and ecosystem function. The broad congruence of these variations with climatic and environmental conditions on local, regional, and global scales has fostered the concept that plant ecophysiological characteristics are well adapted to their local circumstances. For example, the repeated occurrence of plants with CAM (Crassulacean Acid Metabolism) photosynthesis and succulent leaves or stems in severely water-limited environments, and the independent evolution of these traits in numerous plant lineages, provides compelling evidence of the physiological evolution of these water-conserving traits under the influence of natural selection (Ehleringer and Monson 1993). Similarly, studies of the evolution of heavy metal tolerance confirm that natural selection may cause rapid ecophysiological evolution in just a few generations, leading to local adaptation in populations just a few meters apart (Antonovics et al. 1971). Many ecophysiological traits—considered here as all aspects of resource uptake and utilization, including biochemistry, metabolism, gas exchange, leaf structure and function, nutrient and biomass allocation, canopy structure, and growth—are likely to influence fitness and undergo adaptive evolution. Traits affecting the assimilation and use of resources such as carbon, water, and nutrients directly influence plant growth. Patterns of resource allocation to growth, reproduction, defense, and stress tolerance are also likely to be under strong selection. Phenotypic plasticity, the expression of different phenotypes by

Light spectral quality, phytochrome and plant competition.

The light environment experienced by plants in natural vegetation is strongly dependent upon interactions with neighbors. For plants in dense stands, reduced irradiance can lead to reductions in growth and fitness. Spectral light quality is also altered beneath a leaf canopy, and can serve as an important signal of competition for light. Recent physiological studies indicate that plants can perceive the quality of light reflected from neighbors as an accurate predictor of future competition, and respond morphologically even before they are directly shaded. These findings have important implications for plant population biology, and provide a valuable opportunity for the study of adaptive plasticity.

A Test of the Adaptive Plasticity Hypothesis Using Transgenic and Mutant Plants Disabled in Phytochrome-Mediated Elongation Responses to Neighbors

Many plants display characteristic phytochrome-mediated stem elongation responses to crowding and vegetation shade, commonly referred to as the shade avoidance syndrome. We tested the hypothesis that this elongation is a form of adaptive plasticity by comparing the relative performance at high and low density of wild-type plants and transgenic and mutant plants in which the shade avoidance response was disabled. Transgenic tobacco plants in which elongation in response to neighbors was blocked by expression of the oat PHYA gene had decreased relative fitness when grown in competition with elongated wild-type plants. In contrast, constitutively elongated Brassica ein mutant plants, deficient in light-stable phytochrome, had lower fitness relative to nonelongated wild type at low density than in competition with elongated wild type at high density. The observation that phytochrome-mediated elongation is advantageous in dense stands, but disadvantageous for uncrowded plants, indicates that a response to foliage shade allows plants to develop an appropriate morphology for the level of competition they experience. This observation supports the adaptive plasticity hypothesis for this ecologically important trait.

Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs.

Plants shaded by neighbors or overhead foliage experience both a reduction in the ratio of red to far red light (R:FR), a specific cue perceived by phytochrome, and reduced photosynthetically active radiation (PAR), an essential resource. We tested the adaptive value of plasticity to crowding and to the cue and resource components of foliage shade in the annual plant Arabidopsis thaliana by exposing 36 inbred families from four natural populations to four experimental treatments: (1) high density, full sun; (2) low density, full sun; (3) low density, neutral shade; and (4) low density, low R:FR‐simulated foliage shade. Genotypic selection analysis within each treatment revealed strong environmental differences in selection on plastic life‐history traits. We used specific contrasts to measure plasticity to density and foliage shade, to partition responses to foliage shade into phytochrome‐mediated responses to the R:FR cue and responses to PAR, and to test whether plasticity was adaptive (i.e., in the same direction as selection in each environment). Contrary to expectation, we found no evidence for adaptive plasticity to density. However, we observed both adaptive and maladaptive responses to foliage shade. In general, phytochrome‐mediated plasticity to the R:FR cue of foliage shade was adaptive and counteracted maladaptive growth responses to reduced PAR. These results support the prediction that active developmental responses to environmental cues are more likely to be adaptive than are passive resource‐mediated responses. Multiple regression analysis detected a few costs of adaptive plasticity and adaptive homeostasis, but such costs were infrequent and their expression depended on the environment. Thus, costs of plasticity may occasionally constrain the evolution of adaptive responses to foliage shade in Arabidopsis, but this constraint may differ among environments and is far from ubiquitous.

Pollinator foraging behavior and gene dispersal in Senecio (Compositae).

Wright (1943, 1946) showed that in a continuous population of organisms, the pattern of genetic differentiation is largely determined by the number of individuals in a local random breeding unit, or neighborhood. When neighborhoods are small, populations are subject to greater differentiation, both randomly and in response to natural selection. Neighborhood size is a function of population density and gene dispersal. The breeding systems and stationary spatial distributions of animal-pollinated flowering plants are consistent with the assumptions of Wrights models; such systems have proved excellent for the study of neighborhood size, because gene dispersal can be estimated directly by measuring pollinator movements and seed dispersal distances (Kerster and Levin, 1968; Levin and Kerster, 1968, 1969a, 1969b, 1974; Schaal and Levin, 1978; Beattie, 1979). The foraging behavior of pollinators has major importance for patterns of gene dispersal in plant populations (Levin, 1979a, 1979b). Foraging behavior in turn may be affected by the quality and distribution of the nectar sugar rewards offered by flowers (Heinrich and Raven, 1972; Heinrich, 1975). Pollinators can utilize only flower resources which provide sufficient caloric reward to make foraging energetically profitable (Heinrich and Raven, 1972; Heinrich, 1975). Types of pollinators may differ by several orders of magnitude in the metabolic energy costs they incur during foraging and thermoregulation (Heinrich and Raven, 1972; Heinrich, 1975). For example, butterflies, which thermoregulate by basking (Watt, 1968) and have relatively low foraging costs, can profitably utilize flowers with relatively small nectar rewards (Watt et al., 1974), while bumblebees and hawkmoths, which thermoregulate metabolically and expend more energy in foraging (Heinrich, 1975), would operate at a loss on the same resource. Many flower species have specialized features of nectar presentation adapting them to a particular pollinator type (Heinrich and Raven, 1972; Faegri and van der Pijl, 1979). For example, plant species specialized for bumblebee or hawkmoth pollinators often provide rich nectar rewards in deep-spurred nectaries that are inaccessible to low-energy pollinators. On the other hand, many plants provide minute quantities of nectar that are profitable only to animals with low metabolic costs. If pollinator types with different energy requirements differ in their foraging behavior, then the neighborhood structures of plants specialized for those pollinators can be expected to differ also. Linhart (1973) has shown that pollen dispersal patterns in tropical Heliconia differ dramatically depending on whether territorial or traplining hummingbirds are the pollinators. Moreover, for plants which are generalists, pollinated by several types of animals, neighborhood structure may be significantly affected by the proportion of pollen transferred by different pollinator types. Two aspects of pollinator foraging behavior have particular importance for patterns of plant gene dispersal. First, flight distances between plants will determine the distance over which pollen is transferred. Second, in self-compatible plants the number of flowers visited per plant will determine the proportion of seeds set that are selfed or outcrossed, and thus will affect levels of inbreeding. Moreover, if pollen from a given flower is carried over to more than one of the flowers subse-

EVIDENCE OF ADAPTIVE DIVERGENCE IN PLASTICITY: DENSITY- AND SITE-DEPENDENT SELECTION ON SHADE-AVOIDANCE RESPONSES IN IMPATIENS CAPENSIS

We investigated the conditions under which plastic responses to density are adaptive in natural populations of Impatiens capensis and determined whether plasticity has evolved differently in different selective environments. Previous studies showed that a population that evolved in a sunny site exhibited greater plasticity in response to density than did a population that evolved in a woodland site. Using replicate inbred lines in a reciprocal transplant that included a density manipulation, we asked whether such population differentiation was consistent with the hypothesis of adaptive divergence. We hypothesized that plasticity would be more strongly favored in the sunny site than in the woodland site; consequently, we predicted that selection would be more strongly density dependent in the sunny site, favoring the phenotype that was expressed at each density. Selection on internode length and flowering date was consistent with the hypothesis of adaptive divergence in plasticity. Few costs or benefits of plasticity were detected independently from the expressed phenotype, so plasticity was selected primarily through selection on the phenotype. Correlations between phenotypes and their plasticity varied with the environment and would cause indirect selection on plasticity to be environment dependent. We showed that an appropriate plastic response even to a rare environment can greatly increase genotypic fitness when that environment is favorable. Selection on the measured characters contributed to local adaptation and fully accounted for fitness differences between populations in all treatments except the woodland site at natural density.

THE EVOLUTIONARY ECOLOGY OF SEED GERMINATION OF ARABIDOPSIS THALIANA: VARIABLE NATURAL SELECTION ON GERMINATION TIMING

Abstract Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14‐h and 10‐ h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June‐dispersed seeds in RI, but only 4% in November‐dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.

The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis

If microgeographic variation in selection within a natural plant population has resulted in local adaptation, then offspring fitness should decline with distance from the parental site. If outcrossed progeny are less well‐adapted to the parental environment than inbred progeny, but perform better in environments different from that of the parent, then the fitness of inbred progeny relative to outcrossed progeny should decrease with dispersal distance from the parent. To test these predictions, we collected seedlings at 10‐m intervals from a 40 times 40‐m permanent grid in a natural population of Impatiens capensis, grew them in a greenhouse, and crossed them to produce outcrossed chasmogamous seeds. Seedlings from outcrossed chasmogamous and self‐fertilized cleistogamous seeds were planted back into the source population in the original site of their maternal parents and in arcs 3 and 12 m from the parental location and censused weekly for survival and reproduction. The fitness of inbred offspring declined significantly and the magnitude of observed inbreeding depression increased with distance from the parental site, supporting the local adaptation hypothesis.