Elsevier

Acta Oecologica

Volume 27, Issue 3, May–June 2005, Pages 185-195
Acta Oecologica

Original article
Life history responses to irradiance at the early seedling stage of Picea omorika (Pančić) Purkyňe: adaptiveness and evolutionary limits

https://doi.org/10.1016/j.actao.2004.12.004Get rights and content

Abstract

A multivariate selection analysis has been implemented for testing the adaptiveness of life history plasticity to irradiance during the seedling establishment in Picea omorika plants raised in a growth-room. Siblings of a synthetic population comprising 21 families from six natural populations were exposed to contrasting light levels to explore variation in phenotypic expression of three seedling traits: days from germination to cotyledon opening (DGTOC), days from cotyledon opening to epicotyl appearance (DCTOE), and epicotyl length at 6 weeks (EPL6). Ambient light conditions significantly affected DCTOE and EPL6, but not DGTOC. Phenotypic selection analysis revealed that DGTOC was under negative directional selection in both radiation environments, suggesting that canalization of DGTOC was promoted across different light conditions, as well as that the observed pattern of canalization might be regarded as adaptive. DCTOE was also found to be under negative directional selection in both light treatments, but the plastic responses of this trait were opposite to the values favoured by selection within environments. Since there was evidence for selection against plasticity in DCTOE, the pattern of plastic responses in DCTOE to variation in light conditions could be diagnosed as maladaptive. Multiple regression analysis revealed a cost of canalization in DGTOC regardless of light environment, as well as a cost of plasticity in DCTOE under high light intensity. All genetic correlations across light environments were significantly different from unity, indicating the existence of heritable variation for plasticity in these traits. However, since DGTOC and DCTOE were involved in a genetic trade-off with respect to both trait mean and plasticity, these early life histories would never reach their optimal values across radiation environments.

Introduction

As photoautotrophic and immobile organisms, higher plants have evolved an exceptional degree of developmental plasticity in response to multiple informational signals from the light environment, thereby optimizing their developmental patterns in a way that maximizes radiant energy capture, survival and reproduction (Kendrick and Kronenberg, 1994; Nemhauser and Chory, 2002). Plant responses to changing light conditions are the most prominent during seedling establishment, when they are “observable at all levels of organization, from visible phenotype to gene expression” (Quail, 2002, p. 5). During this short window of time, the emerging seedlings respond to the incident radiation by assuming a developmental program that enables them to become quickly photoautotrophic. A plant’s ability to sense specific environmental signals and interpret this information to produce appropriate morphological and developmental changes is facilitated through a suits of informational photoreceptors, characterized by the wavelength of light that they perceive (Quail, 2002; Sullivan and Deng, 2003).

The radiation environments in the wild are very complex, so that most plants simultaneously experience a mixture of light quantities and qualities. Under such conditions, phenotypic variation expressed by individual genotypes in different light environments often reflects both active (anticipatory) plasticity occurring in response to specific informational cues signaling imminent events in the environment and passive (inevitable) environmental effects on the phenotype elicited by low resource levels (Sultan and Bazzaz, 1993; Sultan, 2000; Pigliucci, 2001). Plastic responses to environmental signals are thought to promote functional adjustment to the environment by permitting different genotypes to converge to a single phenotype appropriate for the prevailing environmental conditions or by allowing a single genotype to produce different phenotypes in different environments (Sultan and Bazzaz, 1993; Schmitt et al., 1999; Ackerly et al., 2000; Sultan, 2000). Since the phenotypes induced by each environment are expected to confer high fitness in that environment relative to alternative phenotypes, such plasticity is often regarded as adaptive. Current quantitative genetic models of plasticity evolution predict that as long as the costs of this kind of plasticity are low, suitable genetic variation is available, and strong genetic correlations between the expression of a trait in different environments and/or among different traits within environments are lacking, the shape of a reaction norm should evolve toward the optimal phenotypic value within each environment (Via and Lande, 1985; Schlichting, 1986; Van Tienderen, 1991; De Witt et al., 1998). Conversely, resource-mediated developmental limits are assumed to be ecologically non-functional, and as such are often interpreted as non-adaptive or even maladaptive plasticity (Ackerly et al., 2000; Sultan, 2000). Schlichting and Smith (2002, p. 193) have recently pointed out, however, that there are inevitable responses to suboptimal environmental conditions that “may seem non-adaptive, but over evolutionary time even these seemingly non-functional responses may have been selected as preferred alternatives to more drastic outcomes-such as death”.

In plants, the period of seedling establishment is recognized to be the principal determinant of their competitive success, and ultimately of their expected lifetime fitness (Harper, 1977; Fenner, 1987; Sultan, 1996). Although at this early developmental stage seedling growth hinges profoundly on seed reserves provided by the maternal plant, the effectiveness of functionally appropriate phenotypic responses induced by environmental variation might be strongly influenced by their timing (Sultan, 2000). Many experimental studies show that the time at which seedlings emerge from the soil in natural environments may have strong effect on their performance and survival (Arthur et al., 1973; Howell, 1981; Kalisz, 1986; Miller, 1987). Generally, earlier emerging individuals displayed a higher biomass, and therefore a greater probability of survival. Phenotypic selection analyses on the timing of emergence have detected negative directional selection on this life history trait in different plant taxa, supporting the notion that the earliest emerging individuals indeed display the highest fitness when there is competition for light (Miller, 1987; Dorn et al., 2000; Weinig, 2000; Poulton and Winn, 2002). Since light is a directionally supplied resource which can be pre-empted by larger individuals, competition for light is often asymmetric. Thus, when two plants are competing for light energy, only one will experience reduced light levels. Accordingly, an increased relative fitness of earlier emerging seedlings would be a consequence of density-dependent resource pre-emption, which directly affected their individual size (Miller, 1987; Aarssen, 1995; Schwinning and Weinberg, 1998).

Plants often alter their growth form and functional performance, in order to reduce competitive suppression. In many plant species, and especially in the shade-avoiders, allometric changes are much more important than physiological changes because shade-intolerant individuals can only survive or reproduce if they overtop neighbour plants. This may be achieved if they are among the early emerging individuals, and if they have an elongated growth habit (Miller, 1987; Henry and Aarssen, 1997; Schwinning and Weinberg, 1998). Such shade-avoidance growth strategy is predicted to be “most common in early to intermediate stages of succession, when the probability of encountering high irradiance through vertical growth is still reasonably high” (Henry and Aarssen, 1997, p. 579).

In the present study, we examined the fitness consequences of early life history responses to irradiance in the seedlings of Picea omorika, a shade-intolerant conifer tree species. Natural regeneration of this tree occurs exclusively within disturbed and relatively open habitats such as forest clearings and vegetation gaps, where it predominates as the primary recruit in forest succession (Čolić, 1957, Čolić, 1966). Since the light conditions within the early successional understories are extremely variable—both in space and time, and because the variability in available light occurs at lower vegetation strata, slight differences in plant size may often result in large differences in light energy acquisition (Aarssen, 1995). In the face of such unstable light conditions, the capacity of Pomorika individuals to become rapidly photoautotrophic might indeed be of principal importance for their success in the competition for radiant energy. To test this prediction, we addressed the following questions: (1) How do the ambient light conditions affect the timing of early life history events, such as cotyledon opening and epicotyl appearance in Pomorika seedlings? (2) Does the strength or direction of natural selection on these seedling life-history traits vary with light availability, which is a necessary condition for plastic responses to environmental variation to be regarded as adaptive? (3) Is plastic response to light intensity in the same direction as selection in each light treatment? (4) Does the ability to be plastic or constant for the traits analysed imposes a maintenance cost to Pomorika individuals? (5) Is there sufficient genetic variation in reaction norms of early life-history traits for the evolution of optimal reaction norms to ambient light conditions in Pomorika?

Section snippets

Study species

Pomorika (Pančić) Purkyňe is an endemic conifer tree naturally distributed within a narrow area around the middle and upper courses of the river Drina, at the border between Bosnia and Serbia. Currently, the species consists of several natural populations—about 10 populations differing in size in Bosnia, and about 20, mostly smaller populations, in Serbia. Pomorika is a wind-pollinated outcrossing species, so that ovules produced by an individual tree are fertilized by pollen provided by

Phenotypic responses to irradiance

Apart from cotyledon number, preformed during embryogenesis on the maternal plant, light treatments applied in the present study significantly affected the phenotypic values of all traits analyzed (Table 1). Seedlings experiencing a reduced light level displayed a slightly increased time interval from cotyledon opening to epicotyl appearance, and a significantly prolonged epicotyl appearance rate relative to those raised under high light conditions (Table 1). The length of epicotyl at 6 weeks

Adaptiveness of life history responses to light availability

The early life history traits of Pomorika expressed differential sensitivity to variation in ambient light conditions that prevailed during the first 6 weeks of seedling growth in a growth-room. While the average time from seed germination to cotyledon opening remained similar between different light regimes, the mean number of days from cotyledon opening to epicotyl appearance significantly increased under reduced light intensity comparing to high light intensity. The cotyledon number

Acknowledgments

We are very grateful to the associate editor Jacqui Shykoff and two anonymous reviewer for their constructive comments on the manuscript. This work was supported by the Ministry for Science, Technology and Development of Serbia, Grant # 1570.

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