Other Martin J. Lechowicz Publications

J. Evol. Biol. 1, 255-273. (1988)
Assessing the contributions of multiple interacting traits to plant reproductive success: environmental dependence.
Lechowicz, M.J. and Blais, P.A.

Abstract
The reproductive success of sibling cocklebur plants (Compositae: Xanthium strumarium) was monitored after growth at different levels of availability of water and nutrient resources. Variation in reproductive success among individual plants was related to physiological, structural, and phenological characteristics. Reproductive success increased with increased availability of resources, but the relative contribution of particular traits to reproductive success varied with resource availability. Allocation of biomass to different vegetative tissues, time to seedling emergence, degree of branching, transpiration rates, water use efficiency, the rate of decline in height growth after seedling emergence and final plant size all varied significantly with resource availability. However, the changes in each of these phenotypic traits across three garden environments did not always correlate with reproductive success. The shifts across environments in the apparent importance of somatic traits for reproductive success were attributed to plastic changes in the traits but also to changes in the phenotypic correlations of the traits with reproductive success.

Plant phenotypic plasticity—the Sede-Boker workshop (1998)
Evaluating adaptive plasticity: considerations in a phylogenetic perspective
Martin J. Lechowicz, Department of Biology, McGill University, Montreal, Quebec, Canada.

We can evaluate the generality and adaptive value of plastic responses to an environmental change by comparisons among species set in their phylogenetic context. For a particular phenotypic response to environmental differences to be considered adaptively plastic that response should 1) make functional sense and 2) be phylogenetically structured. In other words, plastic changes among a set of functionally related traits that enhance or at least sustain plant performance in a new environment can be seen as adaptive plasticity, especially if closely related species either behave similarly, or diverge in ways that are consistent with a functional and evolutionary trend in the phylogeny.

In this perspective, I evaluate the adaptive value of responses of diverse species of forest maples (Acer) that have been growing in the simulated shade of a forest understory but then find themselves in a sunnier environment with the death of an overstory tree. This eventuality is commonplace in the ecology of all these maple species and we can expect them to have evolved adaptations to both the understory and the gap environments. Some sort of ecological and evolutionary patterns should emerge in a comparison of the responses of these forest maples to this natural transition from shaded to sunnier conditions.

Three considerations arise in a review of a wide range of ecophysiological and architectural responses of these maples to the shade to sun transition:

1. Patterns of plasticity in functionally important traits among closely related species can be quite disparate. What appears to be adaptive plasticity for one species, may well be maladaptive or selectively neutral for another.

2. To understand the functional and evolutionary biology of plasticity, we may need to reassess the traits that we measure. Some traits, perhaps unrecognized or unappreciated, may well be the foci of the evolution of plant function, including adaptive plasticity. Many traits we measure may be only artifacts or epiphenomena that mislead our inquiry into the evolution of whole plant function. Photosynthetic capacity and alternative measures of growth provide examples.

3. Perhaps we should shift our discussion from plasticity to versatility — not how a trait changes between environments, but rather how a trait functions across its full range of potential environments. Injudicious subsampling of the entire norm of reaction may obscure the functional biology of plant responses to environmental variation.

These considerations touch on the limits to interpretation of adaptive plasticity in isolated traits in single species and suggest the need for a broader view of functional linkages among traits in species of known phylogenetic relationships.

Plant phenotypic plasticity—the Sede-Boker workshop (1998)
Plasticity mechanisms: When the details matter.
Carlos L. Ballaré, IFEVA, Dept. de Ecología, Facultad de Agronomía, Universidad de Buenos Aires, Argentina.

Individual plants acclimate to (and sometimes anticipate) variations in their biotic and abiotic environment using a host of information-acquiring systems. These systems sense informational signals, activate the relevant molecular circuitry and ultimately elicit plastic changes in gene expression and protein function. Plastic responses are continuously implemented in the plant and serve a number of functions, including the maintenance of metabolic homeostasis, foraging for resources, and defense. In most cases plastic responses involve metabolic as well as morphological and developmental components. Therefore, classifying plants as plastic or non-plastic may be risky. Plants from harsh environments may show little morphological plasticity to, for example, light quality variations; however, chances are that they appear to be extremely plastic if one chooses to look at their metabolic responses to rapid variations in nutrient availability.

Although it is not uncommon in ecology textbooks to describe plant responses to environmental stresses as inevitable consequences of limitations or imbalances in the resources available to the plant, it is seldom pointed out that these responses are based on finely-tuned and coordinated information-transduction cascades, and do not necessarily represent the only possible solution to the resource conflicts presented by the environment. Plastic responses are triggered by a variety of signals, including things that are frequently considered only in terms of their energetic value or deleterious effects. Thus, signals that engage specific response programs include: (1) specific external clues (such as changes in the red:far-red ratio, biotic elicitors, etc.), (2) variations in the amount of resources available to the plant (e.g., incident PPFD, hexose level in a particular tissue, etc.), and (3) products of cellular damage (e.g., DNA lesions, free radicals, etc.). Any molecular mechanism that is capable of extracting information from 1, 2, and 3, and transforming that information into a potentially useful plastic response, should be expected to be under continuous selective pressure.

There is growing evidence indicating that different environmental and biotic factors can induce convergent information-transduction chains, which lead to similar plastic responses. For example, plastic responses to several stress factors (chilling, UV, water stress) may involve free radicals as messengers and result in the induction of antioxidant enzymes and enzymes of the phenylpropanoid pathway. It is therefore at least possible that a good part of the molecular circuitry that allows the plant to acclimate to fluctuations in a given environmental factor may have been selected under the combined influence of various environmental factors.

Frequently, the functional details of the mechanisms that allow plants to sense and react plastically to changes in their environment tend to be ignored or overlooked in descriptions of plant responses to competition or to abiotic stresses. Some of the limitations associated with the use of very simple models of plant function will be discussed. For example, it is clear that competition models that are simply based on resource consumption cannot account for plastic, active morphological responses of the plants, which in many environments are critical for the outcome of competition. Similarly, the lack of a mechanistic description of plastic responses to environmental factors will make it difficult to understand why there is cross-acclimation to disparate stress sources, and will certainly limit our ability to design fruitful experiments to understand how plants cope with environmental variation.

BioScience 50(11): 979-995 (Nov. 2000)
The Evolution of Plant Ecophysiological Traits: Recent Advances and Future Directions
David D. Ackerly, Susan A. Dudley, Sonia E. Sultan, Johanna Schmitt, James S. Coleman, C. Randall Linder,
Darren R. Sandquist, Monica A. Geber, Ann S. Evans, Todd E. Dawson, and Martin J. Lechowicz

The adaptive value of ecophysiological traits

An ecophysiological trait can be considered adaptive if it has a direct impact on fitness in natural environments. Here we examine the successes and limitations of varied perspectives from which this problem has been addressed.

Phenotypic selection analysis. The most straightforward evidence for the adaptiveness of ecophysiological traits is the observation of correlations between traits and fitness in natural populations, but this approach has proven problematic. For example, direct correlations between photosynthetic rates and fitness are rarely observed in natural populations (e.g., Farris and Lechowicz 1990 and references). Moreover, even when correlations are observed, it is difficult to determine whether individual traits contribute directly to variation in fitness or whether these relationships reflect indirect selection via correlated traits. For example, a study of Plantago lanceolata found a significant positive correlation between photosynthetic capacity and reproductive dry weight, but correlations were also observed for corm diameter, number of leaves, leaf size, specific leaf weight, and transpiration rate (Tonsor and Goodnight 1997). Thus, it is impossible to say that variation in photosynthetic rate, per se, contributed directly to individual fitness.

*Farris MA, Lechowicz MJ. 1990. Functional interactions among traits that determine reproductive success in a native annual plant. Ecology 71: 548-557.

The first selection study on plant ecophysiological traits was conducted by Farris and Lechowicz (1990), who measured selection on ecophysiological, phenological, morphological, and growth traits in a Xanthium population grown under uniform experimental conditions. They created an experimental population in the greenhouse that maximized genetic variation and then planted seedlings into a garden, preventing any correlation between genotype and microenvironment that could confound the results. Twelve traits on each plant were measured at different times during the season, and path analysis was used to integrate the functional relationships among traits into the selection analysis. The researchers found that seedling emergence time, height and branch growth rates, and water-use efficiency all influenced total vegetative biomass, which in turn was strongly correlated with fitness, illustrating that these traits were under selection.

* Lechowicz M,Wang ZM. 1998. Comparative ecology of seedling spruces: A phylogenetic perspective on adaptation. Page 16. Ecological Society of America, 83rd Annual Meeting, Abstracts.

Lechowicz and Wang (1998) have conducted one of the few studies evaluating phenotypic plasticity in a phylogenetic context (see also Pigliucci et al. 1999). In a study of 16 species of North American spruce growing in ambient and elevated CO2 and low and high water availability, they found that interspecific variation in many morphological and ecophysiological traits was not associated with the species’ phylogenetic relationships. However, relative growth rate, which is the outcome of interactions among many ecophysiological traits, showed consistent evolutionary trends across species. Perhaps most interesting, relative growth rate was also less plastic across environments than the many ecophysiological traits underlying variation in growth, but the levels of plasticity in growth rate did not themselves show any pattern of phylogenetic constraint. Evolution of function in extant spruces has apparently involved different patterns of diversification in the mean value of traits affecting growth and in the plastic expression of these traits in differing environmental regimes.

One of the most important results of such research is the demonstration that patterns of phenotypic variation, its genetic basis, and natural selection vary in different environmental conditions. For example, in the sand-dune annual Cakile edentula, high water-use efficiency and intermediate leaf sizes were correlated with fitness in an environment with low water availability, while larger leaf sizes were favored in an environment with high water availability (Figure 1; Dudley 1996a). In the low-water environment, the finding that genotypes with intermediate leaf size had the highest fitness illustrates the importance of nonlinear approaches in selection studies. This pattern indicates the occurrence of stabilizing selection, in which intermediate trait values are favored, in contrast with directional selection, which favors lower or higher values of a trait. In addition, genetic differentiation between populations derived from low- and high-water environments mirrored the selection results: The low-water population had higher water-use efficiency and smaller leaf size when lines from both populations were raised in a common greenhouse environment (Dudley 1996b).

The interface between intraspecific and interspecific variation provides a critical link between microevolutionary processes within populations and larger patterns of diversification and adaptation. For example, both within and among species of Helianthus, variation in the relative proportions of saturated and unsaturated fatty acids in seed oils parallels climatic differences in the species’ ranges. Experimental studies suggest that within H. annuus, seed oil composition influences germination performance, producing a tradeoff between the timing of germination at low temperature and the rate of growth at high temperature (Linder 2000). This tradeoff suggests that the interspecific biogeographical patterns in seed oil composition of Helianthus species result from selection within each lineage for optimal seed oil composition in its local environment. By studying local adaptation of species with broad geographic distributions, it may be possible to explain how selection has influenced the microevolution of seed oil composition at the level of individual genes. Patterns revealed at this level can then be compared with genetic differences among species with different geographic ranges. Such an approach would indicate whether physiologically important traits become adapted to different environments by the same genetic mechanisms in independently evolving lineages.

Ecological Society of America, 83rd Annual Meeting, Abstracts. Page 16. 1998.
Comparative ecology of seedling spruces: A phylogenetic perspective on adaptation.
Lechowicz M, Wang ZM.

There are some 35 species of spruce (Pinaceae: Picea) worldwide, mostly in north temperate and boreal habitats. Some are widespread and commercially important, others are local endemics. The species vary substantially in their edaphic and climatic distributions. Given the ecological diversity represented and the reasonably well-defined phylogenetic relationships in Picea, the genus lends itself to comparative analyses of adaptation. We will present the results of an analysis of the responses of 16 spruce species grown under factorial combinations of (1) ambient and elevated CO2 and (2) low and high water availability. The species studied represent all the main lines of evolution within the genus. We consider the degree to which the characteristics of the different species represent shared ancestral traits versus possible adaptation to their different contemporary environments.