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Phytochrome-Mediated Shade Avoidance Responses1 INTEGR.COMP.BIOL., 43:459±469 (2003) The Adaptive Evolution of Plasticity: Phytochrome-Mediated Shade Avoidance Responses1 JOHANNA SCHMITT,2 JOHN R. STINCHCOMBE,M.SHANE HESCHEL3 AND HEIDRUN HUBER4 Department of Ecology and Evolutionary Biology, Box G-W, Brown University, Providence, Rhode Island 02912 SYNOPSIS. Many plants display a characteristic suite of developmental ``shade avoidance'' responses, such as stem elongation and accelerated reproduction, to the low ratio of red to far-red wavelengths (R:FR) re¯ected or transmitted from green vegetation. This R:FR cue of crowding and vegetation shade is perceived by the phytochrome family of photoreceptors. Phytochrome-mediated responses provide an ideal system for investigating the adaptive evolution of phenotypic plasticity in natural environments. The molecular and developmental mechanisms underlying shade avoidance responses are well studied, and testable ecological hypotheses exist for their adaptive signi®cance. Experimental manipulation of phenotypes demonstrates that shade avoidance responses may be adaptive, resulting in phenotypes with high relative ®tness in the envi- ronments that induce those phenotypes. The adaptive value of shade avoidance depends upon the competitive environment, resource availability, and the reliability of the R:FR cue for predicting the selective environ- ment experienced by an induced phenotype. Comparative studies and a reciprocal transplant experiment with Impatiens capensis provide evidence of adaptive divergence in shade avoidance responses between woodland and clearing habitats, which may result from population differences in the frequency of selection on shade avoidance traits, as well as differences in the reliability of the R:FR cue. Recent rapid progress in elucidating phytochrome signaling pathways in the genetic model Arabidopsis thaliana and other species now provides the opportunity for studying how selection on shade avoidance traits in natural environments acts upon the molecular mechanisms underlying natural phenotypic variation. INTRODUCTION Measuring natural selection on plastic traits in mul- In coarse-grained heterogeneous environments, the tiple environments, and on plasticity itself, calls for a ability of a genotype to develop different phenotypes combination of approaches. Usually it is necessary to in response to environmental cues of future selective replicate the same genotypes across environments and conditions may be an important performance trait. If measure trait expression as well as ®tness in each en- such phenotypic plasticity results in accurate matching vironment. To test ecological hypotheses about the of phenotype to environment, it may result in high adaptive value of plasticity, it is important to manip- relative ®tness across the range of ecological condi- ulate speci®c environmental factors known to in¯u- tions an organism experiences. Plasticity is therefore ence the expression of the trait (Wade and Kalisz, often assumed to be adaptive. However, to determine 1990; Dudley and Schmitt, 1996; Schmitt et al., 1999). the relationship between plasticity and ®tness, it is nec- However, to measure the natural pattern and frequency essary to determine the optimal phenotype in each rel- of selection on plastic traits may require a ``phyto- evant environment, by measuring selection on the plas- meter'' approach in which experimental individuals or tic traits of interest. If plasticity is adaptive, we expect genotypes are exposed to ambient environmental var- to observe that the phenotype induced by each exper- iation (e.g., Kingsolver et al., 2001; Kingsolver and imental environment will confer high ®tness in that Gomulkiewicz, 2003; Huber et al., 2004). In all cases, environment relative to alternative phenotypes (Dud- it is important to determine the relationship between ley and Schmitt, 1996; Huey et al., 1999). The prob- phenotype and ®tness in each environment. If suf®- lem with testing this prediction is that plasticity often cient phenotypic variation is expressed within environ- prevents the expression of ``inappropriate'' phenotypes ments, phenotypic selection analysis (e.g., Lande and within an environment under natural conditions. Con- Arnold, 1983; Brodie et al., 1995) may be a useful sequently, it is impossible to determine how selection tool. Genotypic selection analysis (Rausher, 1992; would have acted on unexpressed alternative pheno- Mauricio and Mojonnier, 1997; Stinchcombe et al., types in that environment. Thus, testing the adaptive 2002) is even more valuable for experimental studies plasticity hypothesis presents a challenge for experi- of selection on plasticity, because in coarse-grained en- mentalists. vironments, reaction norms are properties of geno- types, not individuals, and selection on plasticity can 1 From the Symposium Selection and Evolution of Performance only be measured at the genotype level. By replicating in Nature presented at the Annual Meeting of the Society for Inte- genotypes within and across environments and per- grative and Comparative Biology, 4±8 January 2003, at Toronto, Canada. forming selection analyses on genotypic values, we 2 E-mail: [email protected] can also ask whether this adaptive plasticity is costly. 3 Present address of M. Shane Heschel is Harvard University Her- If so, we expect that plastic genotypes will suffer re- baria, 22 Divinity Avenue, Cambridge, Massachusetts 02138. duced ®tness relative to less plastic genotypes express- 4 Present address of Heidrun Huber is University of Nijmegen, Experimental Plant Ecology, Toernooiveld 1, 6525 Nijmegen, The ing the same trait mean within an environment (Van Netherlands. Tienderen, 1991; DeWitt et al., 1998). Genotypic se- 459 460 J. SCHMITT ET AL. lection analysis also avoids bias due to environmental environment (Moran, 1992; Kingsolver and Huey, correlations caused by ecological factors simultaneous- 1998; De Jong, 1999; Tufto, 2000; Sultan and Spencer, ly affecting the measured traits and ®tness (Stinch- 2002) and if maintaining the capacity for plasticity is combe et al., 2002). Direct selection on plasticity may not costly (Van Tienderen, 1991; DeWitt et al., 1998). also be measured using a path analysis of selection on The evolutionary outcome will also depend upon the genotypic means incorporating environmental frequen- frequency of different selective environments, as well cies and transition probabilities (Scheiner and Calla- as the extent of gene ¯ow in structured populations han, 1999). (Van Tienderen, 1991; De Jong, 1999; Tufto, 2000; Studies of selection on naturally expressed variation Sultan and Spencer, 2002). Thus, to understand the in multiple environments may offer insight into pat- evolution of adaptive plasticity, we must not only mea- terns and causes of selection on plastic traits. However, sure natural selection on plastic traits across the range there is an important limitation: plasticity will create of natural environments encountered by the study or- a different range of phenotypes, and thus a different ganism, but also evaluate the predictability and fre- opportunity for selection, within each environment quency of those environments. (Kingsolver, 1995b; Dudley, 1996). It is impossible to Here we use phytochrome-mediated ``shade avoid- determine how selection would have acted on alter- ance'' responses of plants to crowding and vegetation native phenotypes that are not expressed within an en- shade as a model system for investigating these issues. vironment. If there is a history of strong selection to- We begin by describing the underlying biology and ward the optimal reaction norm, there may be little ecological context of shade avoidance responses. Sec- remaining genetic or phenotypic variation around the ond, we review recent empirical tests of the hypothesis trait optimum within any environment, and conse- that these responses are a form of adaptive plasticity. quently little opportunity for current selection. In this Third, we discuss factors that may shape the adaptive case, it is useful to extend the range of expressed phe- evolution of plastic shade avoidance in natural envi- notypes within an environment in order to measure ronments. Speci®cally, we ask: Are shade avoidance selection on alternative phenotypes that normally responses costly? What is the frequency of different would not be expressed (e.g., Nylin et al., 1996; King- selective environments in the wild? Fourth, we review solver, 1995a, 1996; Schmitt et al., 1995, 1999; Dud- comparative and experimental evidence for adaptive ley and Schmitt, 1996; Baldwin, 1998). This extension divergence in shade avoidance responses within and may be accomplished by direct manipulation of a trait among species. Finally, we suggest directions for fur- (e.g., Kingsolver, 1996), by manipulation of the envi- ther research. ronmental cue that elicits expression of alternative phenotypes (Kingsolver, 1995a; Dudley and Schmitt, SHADE AVOIDANCE RESPONSES IN PLANTS: 1996, by application of regulatory substances that me- AMODEL SYSTEM diate a developmental pathway to elicit alternative As any gardener who has waited too long to thin phenotypes (e.g., Van Hinsberg, 1997; Baldwin, 1998; the seedlings knows, crowding in many plant species Cipollini and Schultz, 1999), or by genetic manipula- elicits a suite of developmental responses, such as stem tion of speci®c loci involved in environmental cue per- and petiole elongation, branch suppression, and accel- ception and transduction, or regulated by speci®c sig- erated
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