REVIEW AND SYNTHESIS Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions Christina L. Richards*, Oliver Bossdorf, Norris Z. Muth, Jessica Gurevitch and Massimo Pigliucci Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences, Stony Brook, NY 11794-5245, USA *Correspondence: E-mail: richards@life.bio.sunysb.edu Abstract Invasion biologists often suggest that phenotypic plasticity plays an important role in successful plant invasions. Assuming that plasticity enhances ecological niche breadth and therefore confers a fitness advantage, recent studies have posed two main hypotheses: (1) invasive species are more plastic than non-invasive or native ones (2) populations in the introduced range of an invasive species have evolved greater plasticity than populations in the native range. These two hypotheses largely reflect the disparate interests of ecologists and evolutionary biologists. Because these sciences are typically interested in different temporal and spatial scales, we describe what is required to assess phenotypic plasticity at different levels. We explore the inevitable tradeoffs of experiments conducted at the genotype vs. species level, outline components of experimental design required to identify plasticity at different levels, and review some examples from the recent literature. Moreover, we suggest that a successful invader may benefit from plasticity as either (1) a Jack-of-all-trades, better able to maintain fitness in unfavourable environments (2) a Master-of-some, better able to increase fitness in favourable environments or (3) a Jack-and-master that combines some level of both abilities. This new framework can be applied when testing both ecological or evolutionary oriented hypotheses, and therefore promises to bridge the gap between the two perspectives. Keywords Adaptive evolution, adaptive phenotypic plasticity, ecological genetics, experimental design, fitness homeostasis, general-purpose genotype, genetic assimilation, genotype- environment interaction, invasiveness, molecular markers. Ecology Letters (2006) 9: 981���993 IN T R OD U C TI ON The number of plant species moved by humans across biogeographic barriers has increased dramatically in the last two centuries (Vitousek et al. 1996 Mack et al. 2000). Some of these species become extremely abundant in their new range, and cause major environmental and economic problems (Wilcove et al. 1998 Pimentel et al. 2000). Although interest in preventing and controlling such biological invasions has led to an explosion of scientific studies over the past decades, satisfactory explanations of differential introduction success remain elusive. One mech- anism that has been frequently suggested in the context of plant invasions (Baker 1965 Rice & Mack 1991 Sexton et al. 2002 Sultan 2004), but has been infrequently investigated empirically, is phenotypic plasticity, the property of a genotype to express different phenotypes in different environments (Bradshaw 1965 Schlichting 1986 Scheiner 1993 Pigliucci 2001, 2005). Results from phenotypic plasticity studies indicate that plasticity could play an important role in invasions. In particular, many studies argue that plasticity enhances ecological niche breadth because plastic responses allow organisms to express advantageous phenotypes in a broader range of environments (Bradshaw 1965 Van Valen 1965 Whitlock 1996 Sultan et al. 1998a,b Donohue et al. 2001 Sultan 2001 Richards et al. 2005). Recent studies also suggest that the evolution of plasticity in response to a set of environments may be beneficial in novel sites after colonization or migration (Agrawal 2001 Donohue et al. 2001, 2005 Etterson 2004 Yeh & Price 2004). Ecology Letters, (2006) 9: 981���993 doi: 10.1111/j.1461-0248.2006.00950.x �� 2006 Blackwell Publishing Ltd/CNRS

Invasion biologists refer to phenotypic plasticity in two distinct ways when attempting to explain plant invasions. Based on the arguments above ��� either explicitly or implicitly ��� they have posed two main hypotheses: (1) Invasive species may be more plastic than non-invasive or native ones (e.g. Marshall & Jain 1968 Williams et al. 1995 Durand & Goldstein 2001 McDowell 2002). This idea dates back to the ��general-purpose genotype�� of Baker (1965), who suggested plasticity as one characteristic of an ��ideal weed��. (2) Populations in the introduced range of an invasive species may evolve greater plasticity than populations in the native range (e.g. Kaufman & Smouse 2001 Sexton et al. 2002 Parker et al. 2003). If genetic variation for plasticity exists in introduced populations, and genotypes with more plasticity have a fitness advantage in the novel environment, this will cause evolution of increased plasticity. Generally, rapid evolutionary change appears to be common in invasive species (Brown & Marshall 1981 Thompson 1998 Mooney & Cleland 2001 Sakai et al. 2001 Lee 2002 Bossdorf et al. 2005), and rapid evolution of plasticity could play an important role in explaining their success. Clearly, these two hypotheses reflect to some extent the disparate interests of ecologists and evolutionary biologists. Whether one is interested in cross-species comparisons or microevolution, there are two primary scenarios which describe how a different reaction norm might contribute to invasion success: (1) a Jack-of-all-trades situation, where through the plasticity of morphological or physiological traits, the invader is better able to maintain fitness in a variety of environments (2) a Master-of-some situation, in which the plasticity of morphological or physiological traits allows the invader to take advantage of favourable environ- ments in addition, an invader might be (3) a Jack-and- master that combines some of both of these abilities. While each of these scenarios has been repeatedly mentioned in the literature, it is often not clear to which one invasion biologists are referring when they claim that some species or populations are ��more plastic�� than others. However, it is important to make this distinction explicitly because each scenario makes different predictions about the shape of the reaction norms of invaders, relative to that of the respective controls. In this review, we summarize the hypotheses about how plasticity might contribute to the success of invasive plants, and we outline what is necessary to test these hypotheses. We note that greater phenotypic plasticity is one of many possible hypotheses about the causes of invasion success in plants. The aim of this paper is not to advocate plasticity as the explanation for invasions, but to summarize existing ideas and discuss their conceptual and methodological basis as well as the evidence necessary to test them. To illustrate the different approaches, we use some examples from the recent literature on plasticity in invasives. However, our review is by no means meant to be exhaustive. We briefly review the literature, evaluate the experimental evidence, and identify some promising questions for future research. Moreover, the concept of phenotypic plasticity has often been used imprecisely, and sometimes incorrectly, in this context. Therefore, clarification of some conceptual and methodological issues is needed before we can explore the role of plasticity in plant invasions. T H E C O N C EP T OF P H E N O T Y P I C P L A S T I C I T Y All the conceptual and empirical progress of the last decades notwithstanding, it is still common to encounter basic misconceptions about plasticity whenever the topic comes up for discussion. One such misconception is to view plasticity as an ��alternative�� to genetic variation (see Macdonald & Chinnappa 1989 Pigliucci 2001). Plasticity is a trait ��� a property of a genotype ��� which can be visualized graphically as a pattern of expression in different environments (called a reaction norm). Like other traits, plasticity is subject to evolution by natural selection. Therefore, this dichotomy makes little sense. Phenotypic plasticity refers to the potential of specific traits of a genotype to respond to different environments. This property can affect the performance and reproductive success of individual organisms, which in turn will impact the make-up of the next generation and thus contribute to evolution by natural selection. Because phenotypic plasti- city is a property of specific traits in specific environments, it is incorrect to think of an organism or genotype as a whole as being more or less ��plastic�� than others. A given genotype may be plastic for a certain trait in a certain set of environments, but not plastic for other traits in the same set of environments, or for the same trait in a different set of environments (Bradshaw 1965 Sultan 1995 Pigliucci 2001). A special case that causes much confusion is the plasticity of fitness vs. non-fitness traits. Plasticity of morphological and physiological traits is unlikely to have any effect on invasiveness unless that plasticity contributes to fitness (Fig. 1). Natural selection will generally act to maintain high levels of fitness across environments. We can visualize a fitness reaction norm across environments and refer to changes in fitness across environments as ��plasticity in fitness��. The resulting most favourable reaction norm for fitness, may be invariable or flat (fitness homoeostasis Hoffmann & Parsons 1991 Rejma ��nek 2000). Often, this type of flat fitness reaction norm may be achieved through plasticity in underlying morphological or physiological traits that influence fitness (Bradshaw 1965 Sultan 1995 e.g. Sultan et al. 1998b). In an effort to address this confusion, Fig. 1 illustrates the relationship between fitness traits and other morphological and physiological traits. In this figure, 982 C. Richards et al. Review and Synthesis �� 2006 Blackwell Publishing Ltd/CNRS