Research Projects Pamela K. Diggle Overview Plasticity of morphological characters is an inherently developmental phenomenon. Nevertheless, the role of development in the evolution and expression of phenotypic plasticity has been virtually ignored. My research examines the role of development in the evolution and expression of phenotypic plasticity in plants. The central goal of this research program has been to examine the combined effects of genotype, environment, and ontogenetic history on the development and expression of plant phenotypes. This research has three inter-related foci: 1) determination of developmental constraints on the potential for expression of phenotypic plasticity in plants with morphological preformation; 2) construction of developmental models to distinguish between true phenotypic plasticity and architectural (positionally contingent) effects on phenotypic expression in metameric organisms; 3) investigation of the origin and evolutionary diversification of plastic sex expression in andromonoecious Solanum. These projects are described briefly below.   Preformation and Plasticity in Alpine Tundra Perennials The development of many perennial plants is characterized by preformation, the initiation of structures one or more years before they fully mature and function, a phenomenon absent in annuals and most short lived perennials. I investigated the hypothesis that preformation can inhibit or even preclude the expression of morphological plasticity. Developmental and architectural analyses of Polygonum viviparum (Polygonaceae), an herbaceous perennial of the alpine tundra, resulted in a complete temporal model of the developmental dynamics of this organism (Diggle 1997a). Each leaf and inflorescence borne by an individual is preformed and requires a four-year period of development from initiation to maturation and function. This developmental model of P. viviparum was then used to make explicit predictions about potential short and long term phenotypic responses to environmental variation. Recent analyses in the alpine tundra (at the Niwot Ridge NSF LTER Research Site) demonstrate a delay of one or more years in community level plant responses to environmental variation. A central unresolved issue for alpine ecologists had been to link observed community level responses in the alpine to processes manifest at the level of individuals. Developmental models provide the critical link: as a consequence of the prevalence of extreme preformation in the alpine, developmental responses to environmental change are not "expressed" for an additional one to four years, when those preforming organs mature and function (Diggle 1997a). Studies of the connections between organismic patterns of development and community level response to the environment in the alpine are continuing. In collaboration with two of my graduate students, investigations of preformation, and the constraints of preformation on plasticity, have been extended to other species (Aydelotte and Diggle 1997, Meloche and Diggle, 2001). Manipulative experiments have also tested the mechanistic link between preformation and the delayed response to environmental variation observed in the alpine. Experimental defoliation was used to dramatically alter the resource environment of individuals of both P. viviparum and Caltha leptospeala (Ranunculaceae) (Aydelotte and Diggle 1997, Diggle in preparation). Despite the presence of numerous preformed leaf primordia within the apical bud, neither species is able to replace the photosynthetic tissue lost to defoliation within the growing season. Plants did respond developmentally to the defoliation treatment, however all responses occurred in leaf and inflorescence primordia developing below-ground in the apical bud. The responses were not manifest on an ecological (or mature phenotypic) scale, until one and two years following the treatment. These experiments confirm the importance of developmental models for understanding patterns of response observed at ecological scales. Investigations of Acomastylis rossii (Rosaceae) have shown that the complex morphology, including the presence of a well developed preformed bud bank can ameliorate the constraints imposed by preformation (Meloche and Diggle, submitted). Finally, we have extended our work in the alpine to examine levels of genetic variation within populations. Genetic variation among individuals in the alpine has been predicted to be low due to the prevalence of asexual reproduction. However, during the course of our developmental analyses of plants in the alpine, we discovered that there is considerable phenotypic variation among individuals. This in turn suggested that genetic variation might be significantly greater than expected. An isozyme analysis of P. viviparum confirmed that genotypic diversity in this species is much greater than had been predicted; and may serve as a reservoir for continued population-level responses to environmental fluctuation (Diggle et al. 1998).   Phenotypic Plasticity and Architecture In previous research on the andromonoecious species Solanum hirtum (Solanaceae), I demonstrated that sex-expression, the proportions of hermaphrodite and staminate flowers borne by an individual, is phenotypically plastic and that there is genotypic variation for phenotypic plasticity. During the period of the NYI Award I reconsidered these data and developed my ideas and understanding of the importance of plant architecture and indeterminate development for understanding the expression and the evolution of phenotypic plasticity in plants. In S. hirtum, although the mechanism of plasticity of sex expression resides at the level of gynoecial development of individual flowers, plasticity of sex expression cannot be fully understood by examining flower development in isolation. The particular phenotypic expression of a flower (and by extension, any plant part) depends jointly on two factors: the developmental history (which will reflect the history of both the external and internal environment) of the individual that bears it, and the position of that plant part within the architectural ground plan of the plant. I introduced the terms "ontogenetic contingency" to describe the joint effects of these two factors on phenotypes and "architectural effects" to describe intra-individual phenotypic variation that can be ascribed solely to differences in position (Diggle 1994, 1995, 1997b). Recognition of the critical importance of architectural effects in determining the expression of plasticity in S. hirtum inspired a search for additional evidence of the effects of architecture on reproductive phenotypes in plants. My efforts to examine the broader implications of the effects of architecture and plasticity on plant phenotypes resulted in an invited article published in the Annual Review of Ecology and Systematics (Diggle 1995). In this paper, I circumscribed the concept of architectural effects in greater detail and showed that many of the patterns of resource allocation that are generally attributed (in the literature) to plastic responses to resource competition, may be due, in part or whole, to architectural effects. For example, the commonly observed proximal to distal decrease within inflorescences of fruit and/or seed maturation per flower has frequently been attributed to competition among developing fruits for resources. However, the observed variation can also be due to architecture--that is, to sources of variation inherent in plant axes. Most significantly, I demonstrated that the effects of architecture are separable experimentally from the effects of differential resource allocation, and that careful experimental analysis of these two factors is critical to understanding the physiological, developmental, and evolutionary controls of fruit and seed production in flowering plants. The hypothesis of ontogenetic contingency emphasizes that both architecture and developmental history determine phenotypes. In any analysis of phenotypic plasticity in metameric organisms, it is critical to separate these two factors; only developmental history incorporates plastic responses to the environment. I have formalized an experimental and analytical design to separate plasticity from architectural effects (Diggle 1997b). This design has been used in an analysis of floral characters in S. hirtum, two ecotypes of Arabidopsis thaliana (Diggle 1997b), and Epilobium clavatum (unpublished). I show that architectural effects are extremely common in flowering plants and that architectural effects can mimic, mask, or even cause misinterpretation of plastic variation in floral phenotypes. Finally, I have begun to consider the importance of architecture in the evolution of such life history features as the timing of reproduction. In a literature review (Diggle 1999), I show that architectural features of plants can constrain options for variation in the onset of flower production.   Origin and Evolutionary Diversification of Andromonoecy One of the most intriguing aspects of plant reproductive and evolutionary biology today is the diversity of sexual systems in flowering plants. The majority of flowering plants are hermaphroditic; with each flower bearing both male and female parts. A significant number of flowering plants, however, have evolved highly complex sexual systems that involve the production of different flower types by the same individual. Andromonoecy is a sexual system in which plants produce both hermaphrodite and functionally male flowers. Despite over a century of intensive study of the function of andromonoecy, the origin of this sexual system remains a mystery. This study addresses the evolutionary origin and diversification of andromonoecy within the genus Solanum. This research will identify the specific features of plants and flowers that have been modified during the evolutionary transition from the production of only hermaphroditic flowers to andromonoecy and the ability to produce both hermaphroditic and male flowers. This research on the evolution and function of plant sexual systems has broad implications for basic and applied research in plant biology. Sexual systems determine patterns of mating, and thus the genetic structure of populations. They are important determinants of reproductive output (e.g., fruit production), and may provide critical mechanisms for plant response to environmental variation. The results of this research will be particularly important for understanding past evolutionary responses to a variable environment and predicting mechanisms of response to future environmental change. In addition, functional andromonoecy limits productivity in many species , including perennial fruit crops. This research has the potential to identify developmental processes that can be targeted by breeders and geneticists to improve productivity.

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