Pamela K. Diggle

Extreme preformation in alpine Polygonum viviparum: an architectural and developmental analysis.

Preformation, the initiation of organs one or more years prior to maturation and function, is reported to be common and crucial for plant survival in arctic and alpine environments, yet the phenomenon is remarkably little studied. In order to understand the role of preformation in the ecology and evolution of tundra species, this investigation takes a developmental and architectural approach to the analysis of plant growth and reproduction in the alpine perennial Polygonum viviparam L. Analyses show that the extent and duration of preformation in P. viviparam are extraordinary. Four years are required for each leaf and inflorescence to progress from initiation to functional and structural maturity. This single salient feature of development has profound consequences for basic architecture, dynamics of resource allocation, and the timing of plant responses to environmental variation. As a consequence of the protracted duration of leaf and inflorescence development, five cohorts of primordia, initiated in successive years, are borne simultaneously by an individual plant. In the year prior to maturation leaves reach 30% of their maximum size, and the maximum potential reproductive output of each inflorescence is determined. Thus, developmental processes that affect final morphology and resource allocation occur at least 1 yr before functional maturity. From the developmental and architectural models constructed for P. viviparum, a 1-yr delay in measurable plant responses to environmental variation is predicted. The models also apply generally to arctic and alpine species and provide a mechanistic explanation for observed patterns of productivity at the community and ecosystem scale.

Ontogenetic Contingency and Floral Morphology: The Effects of Architecture and Resource Limitation

Floral form and function commonly vary quantitatively and qualitatively within inflorescences. Overall floral size, the sizes of individual floral organs, and the frequency of successful fruit and/or seed maturation may decline distally within inflorescences. These frequently observed patterns of variation have been attributed to competition for limited resources among developing flowers and fruits. The variation, however, can also be due to architecture, that is, to sources of variation inherent in plant axes. Floral morphology may change with position on an inflorescence axis, even in the absence of resource competition. Experimental analyses of Solanum hirtum and Arabidopsis thaliana identify the separate effects of architectural and resource limitation on floral development and morphology. The effects of architecture may mimic, mask, or lead to misinterpretation of the effects of resource competition on floral form. Floral morphology and function may be characterized as ontogenetically contingent: the morphology and fate of a developing flower depend on the events that have preceded it during the ontogeny of the organism and on where it occurs within the architecture of the individual. Careful consideration of the role of ontogenetic contingency in diverse taxa will be required to fully understand patterns of variation in floral morphology and function within individuals and may ultimately enhance our understanding of morphological diversification among taxa.

Multiple developmental processes underlie sex differentiation in angiosperms

The production of unisexual flowers has evolved numerous times in dioecious and monoecious plant taxa. Based on repeated evolutionary origins, a great variety of developmental and genetic mechanisms underlying unisexual flower development is predicted. Here, we comprehensively review the modes of development of unisexual flowers, test potential correlations with sexual system, and end with a synthesis of the genetics and hormonal regulation of plant sex determination. We find that the stage of organ abortion in male and female flowers is temporally correlated within species and also confirm that the arrest of development does not tend to occur preferentially at a particular stage, or via a common process.

The evolution of unisexual flowers: morphological and functional convergence results from diverse developmental transitions

Unisexual flower morphology was examined within a phylogenetic context in order to identify developmental transitions associated with the multiple origins of dioecy in flowering plants. Historically, two categories of unisexual flowers have been recognized: type I flowers exhibit rudiments of the nonfunctional organ type, while type II flowers bear no vestigial sexual organs. Mapping of these flower types onto a composite phylogeny shows that type II morphology is homoplasious and has resulted from at least four distinct evolutionary developmental pathways. The historical assignment of unisexual flowers into only two morphological types has masked important developmental and evolutionary dynamics.

A developmental morphologist's perspective on plasticity

This series of essays addresses plasticity from the perspective of developmental morphology. The first essay deals with the problem of distinguishing between plasticity and other types of ontogenetic variation. In a temporally varying environment, morphological plasticity may be expressed as the production of a succession of different metamers. However, even in a constant environment, plant metamers can vary dramatically, a phenomenon known as heteroblasty. Because heteroblasty and plasticity can yield similar patterns of ontogenetic variation, the two are often confounded in analyses of developmental plasticity. The second essay discusses the integration of plant phenotypic responses and finds that the evidence for integration is equivocal. The third section shows that developmental properties can constrain the expression of morphological plasticity. Developmental lags and the ‘epiphenotype problem’ are particularly important features for analyses of the evolution and expression of plasticity. Finally, in answer to the question of strategies for studying plasticity, I emphasize the need for research at multiple levels and for the inclusion of a historical or phylogenetic perspective.

CLONAL DIVERSITY IN ALPINE POPULATIONS OF POLYGONUM VIVIPARUM (POLYGONACEAE)

Asexual reproduction is extremely common among arctic and alpine species, and successful sexual reproduction may be rare. In asexual populations, the absence of segregation and recombination predicts reduced levels of genetic variation. Thus, genetic diversity within arctic and alpine plant populations may be quite low. Allozyme analysis of three alpine populations of Polygonum viviparum, a common herbaceous perennial with no observed sexual reproduction, revealed surprising levels of genetic diversity. There were 23 unique clones within a sample of 150 ramets. Few clones were large or distributed among all three sample populations; the majority of clones was rare (n ≤ 5) and unique to a single population. Genotypic diversity differed among the three sample populations. The number of clones and measures of diversity and evenness were much lower in the fell-field population than in wet meadow and dry meadow populations. Overall, genotypic diversity and structure of alpine P. viviparum are similar to other clonal species in which sexual reproduction is rare, and they are similar to the average for clonal species in general.

Mechanisms of differential pollen donor performance in wild radish, Raphanus sativus (Brassicaceae)

In order to understand the characters on which sexual selection might operate in plants, it is critical to assess the mechanisms by which pollen competition and mate choice occur. To address this issue we measured a number of postpollination characters, ranging from pollen germination and pollen tube growth to final seed paternity, in wild radish. Crosses were performed using four pollen donors on a total of 16 maternal plants (four each from four families). Maternal plants were grown under two watering treatments to evaluate the effects of maternal tissue on the process of mating. The four pollen donors differed significantly in number of seeds sired and differed overall in the mating characters measured. However, it was difficult to associate particular mechanistic characters with ability to sire seeds, perhaps because of interactions among pollen donors within styles or among pollen donors and maternal plants. The process of pollen tube growth and fertilization differed substantially among maternal watering treatments, with many early events occurring more quickly in stressed plants. Seed paternity, however, was somewhat more even among pollen donors used on stressed maternal plants, suggesting that when maternal tissue is more competent, mating is slowed and is more selective.

The genetics of floral development differentiating two species of Mimulus (Scrophulariaceae)

Investigation of the developmental processes responsible for the evolution of the small-flowered, highly selfing Mimulus micranthus from its large-flowered, mixed-mating progenitor M. guttatus, revealed M. micranthus to have both a shorter duration and a higher rate of bud development. Hence flowers of M. micranthus can be considered as progenetic forms of M. guttatus. Genetic analysis of F1, F2 and backcross generations derived from the cross M. micranthus × M. guttatus provided no evidence for major gene control of development processes responsible for differentiating the two taxa. Furthermore, F2 segregation patterns suggest that duration and rate of development may be genetically independent of one another. Hence, the evolution of small-flowered selfing taxa in Mimulus may reflect selection for rapid development.

Diversification of andromonoecy in Solanum section Lasiocarpa (Solanaceae): the roles of phenotypic plasticity and architecture

Quantitative analyses of sexual expression show extensive interspecific variation in the strength of andromonoecy (proportions of hermaphroditic and staminate flowers) among Solanum species in the monophyletic section Lasiocarpa. The roles of phenotypic plasticity and inter- and intra-inflorescence architecture in the diversification of andromonoecy within this small clade were analyzed. Four species that represent a range of expression of andromonoecy were examined. Staminate flowers produced within inflorescences ranged from 3% (S. candidum) to 7% (S. ferox) in weakly andromonoecious species and from 39% (S. pseudolulo) to 60% (S. quitoense) in more strongly andromonoecious species. Manipulation of fruit set on clonal replicates of multiple genotypes demonstrated variation among species for phenotypic plasticity. The strongly andromonoecious species, S. pseudolulo and S. quitoense, were not plastic and produced a large proportion of staminate flowers regardless of fruiting treatment, whereas S. candidum and S. ferox were phenotypically plastic and produced significantly more staminate flowers in the presence of developing fruit. Staminate flower production of all four species varied both within and among inflorescences. A greater proportion of staminate flowers were produced in distal (later produced) inflorescences. Within inflorescences, hermaphroditic flowers occurred in basal positions, whereas staminate flowers, when produced, occurred more distally. This pattern of staminate flower production is qualitatively the same in all species investigated; however, quantitative variation in the transition from hermaphroditic to staminate flower production within and among inflorescences is associated with variation in the strength of andromonoecy. At least three factors have contributed to the diversification of andromonoecy in section Lasiocarpa including the presence or absence of phenotypic plasticity in response to fruit set, quantitative variation in intra- and inter-inflorescence architectural effects, and total flower production.

Heteroblasty and the Evolution of Flowering Phenologies

Flowering phenologies have rarely been examined from a developmental perspective. The production of a flower or inflorescence, however, is an integral part of the ontogeny and architecture of an organism. As a result, basic features of plant developmental morphology have the potential to define options for variation in phenology and to determine, in part, the consequences of this variation for other life‐history traits. Two interrelated models of morphological evolution are applied to the analysis of variation in phenology. These models identify the developmental processes of dissociation and addition/deletion as potentially powerful mechanisms of change in the timing of flower production. As a consequence of heteroblasty and architectural features of plant shoots, however, changes in flowering time that occur via dissociation and addition/deletion result inevitably in altered vegetative morphology. If these vegetative characters influence fitness, then response to selection for earlier or later flowering is potentially constrained. A review of the available literature shows that dissociation and addition/deletion do occur in association with changes in flowering phenology. Additional studies that integrate developmental and evolutionary approaches are required to determine the extent to which whole‐plant or shoot‐level developmental and morphological properties may enhance or constrain phenological evolution.