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Phenotypic Plasticity in the Interactions and Evolution of Species Anurag A

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Phenotypic Plasticity in the Interactions and Evolution of Species Anurag A S C I E N C E ’ S C O M P A S S ● R E V I E W R E V I E W : E C O L O G Y Phenotypic Plasticity in the Interactions and Evolution of Species Anurag A. Agrawal species represents an interaction norm where When individuals of two species interact, they can adjust their phenotypes in response the response of one species to the other cre- to their respective partner, be they antagonists or mutualists. The reciprocal pheno- ates the environment to which the other spe- typic change between individuals of interacting species can reflect an evolutionary cies may then respond (Fig. 3). The current response to spatial and temporal variation in species interactions and ecologically sign, strength, and variability in the species result in the structuring of food chains. The evolution of adaptive phenotypic interaction then depends on the past recipro- plasticity has led to the success of organisms in novel habitats, and potentially cal responses between the individuals. In this contributes to genetic differentiation and speciation. Taken together, phenotypic simplified view, spatial aspects of the biotic responses in species interactions represent modifications that can lead to reciprocal and abiotic environment are assumed to be change in ecological time, altered community patterns, and expanded evolutionary constant. The decomposition of the environ- potential of species. mental component of the interaction norm into temporal (Fig. 3) and spatial aspects allows for a more detailed analysis of varia- henotypic plasticity is the ability of an Reciprocal phenotypic change in spe- tion in species interactions. organism to express different pheno- cies interactions. The intersection between Reciprocal phenotypic change in ecologi- Ptypes depending on the biotic or abiotic species interactions and phenotypic plasticity cal time may be (i) a primary determinant of environment (Fig. 1). Single genotypes can has generated considerable interest among an organism’s phenotype in nature; (ii) the change their chemistry, physiology, develop- evolutionary ecologists (Table 1). The study result of long-term evolution where the envi- ment, morphology, or behavior or in response of phenotypic responses of one organism to ronment (i.e., the species interaction) has to environmental cues. R. A. Fisher and other another is by definition an investigation of a been variable; and (iii) a stabilizing factor in 20th century evolutionary biologists lacked species interaction. Yet, biologists have al- mutualistic interactions. A signature of recip- explanations for phenotypic plasticity (1). most entirely focused on plasticity in species rocal phenotypic change is the escalation of Evolutionary biologists have been interested interactions as one-sided events: What is the phenotypes between individuals of two spe- in studying the genetic basis of phenotypes, effect of variation in species X on the pheno- cies over an extended bout of interactions. and early work was focused on traits pre- type of species Y? In nature, however, it is This can be a directional change in the phe- sumed to be unaffected by the environment. quite likely that interacting individuals are notype of partners, where exposure to certain Environmentally affected phenotypes were continually responding to their interaction cues activates genes in a dose-dependent considered of lesser importance because of partners in a reciprocal fashion over ecolog- manner (Fig. 3). For example, in a mutualis- their apparent lack of a genetic basis. The ical time (Fig. 2). Reciprocal interaction sim- tic interaction, individuals may increase re- modern view of phenotypic plasticity rejects ply implies a back-and-forth response in wards in response to increased services from this notion because phenotypic plasticity of- terms of phenotypic change between individ- a partner, and this back-and-forth changing of ten has a genetic basis. Now, many ecologists uals, and does not imply symmetry in the phenotypes can be a continuous or iterative and evolutionary biologists have embraced strength of responses or effects of one partner process. However, reciprocal phenotypic the idea that under many circumstances such on the other. Many antagonistic or mutualis- change does not have to be directional (5–7). phenotypic plasticity can be adaptive (2). tic interactions, including those that are not Here again, there is an analogy to coevolu- This hypothesis parallels Lamarck’s First behavioral, may involve reciprocal phenotyp- tionary dynamics, where two possible out- Law proposed in Philosophie zoologique in ic changes in ecological time. As an analog, comes are escalating (directional) arms races 1809 (3), which stated that organisms accli- studies of coevolution have long attempted to or polymorphisms that are stable or fluctuat- mate to their environment to improve perfor- study the reciprocal evolutionary change in ing in space or time. The latter case predicts mance. Of course, Lamarck is largely dis- interacting species. high levels of genetic and phenotypic varia- credited by his Second Law, which suggested Thompson (4) proposed a similar exami- tion between populations of the interacting that these adjustments to the environment nation of phenotypic plasticity in species in- species because of variation in the cost- were heritable. The modern view of plasticity teractions termed an interaction norm. An benefit ratio of a particular adaptation to can be generalized to the statement that phe- interaction norm is expressed as a genotype- the partner (8). Nondirectional phenotypic notypic plasticity evolves to maximize fitness by-genotype-by-environment interaction. In changes in ecological time may similarly in variable environments (the adaptive plas- other words, the phenotype of an individual result in variable phenotypes between dif- ticity hypothesis) (2). Here, I take the adap- or the sign and strength of an interaction ferent pairs of interacting species. Recent tive plasticity hypothesis as a starting point between species is determined by the geno- advances in the understanding of transpos- for evaluating ongoing and future research types of interacting individuals and the envi- able elements suggest that stress-induced directions in the ecology and evolution of ronmental conditions in which they occur. I retrotransposons may be a mechanism for species interactions. propose a refinement of the interaction norm nondirectional change. Defensive respons- concept that distinguishes environmental ef- es in plants and animals result in increased fects that are generated by spatial versus tem- transpositional activity that may result in Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada. E- poral variation. Reciprocal phenotypic immunity to parasites (6, 7). mail: [email protected] change between individuals of interacting Although studies have not been conducted www.sciencemag.org SCIENCE VOL 294 12 OCTOBER 2001 321 S C I E N C E ’ S C O M P A S S to test the specific hypothesis of reciprocal quently produce tubules. After additional re- strength of predaceous crabs: crabs eating phenotypic change in ecological time, several ciprocal signaling, rhizobia differentiate into mussels without shells grew smaller and examples suggest that it is common. Interac- bacteroids that fix atmospheric nitrogen. Sub- weaker claws than crabs eating intact mussels tions between probable mutualists such as sequent reciprocity dictates the level to which with shells. Conversely, mussels respond to leguminous plants (Fabaceae) and nitrogen- legumes and rhizobia cooperate and ex- cues from predators, including crabs, by in- fixing bacteria (rhizobia) demonstrate recip- change resources (10). ducing increased shell thickness, abductor rocal phenotypic change (9). Bacteria near Reciprocal phenotypic change has also muscle strength, and byssal threads (12, 13). roots start by producing lipo-oligosaccharides been indicated in largely antagonistic interac- In the relationship between plants and herbi- (termed Nod factors). Plants then distort root tions. Smith and Palmer (11) elegantly dem- vores, plants may induce defenses that are hairs that curl around the bacteria and subse- onstrated plasticity in morphology and claw dependent on the density of attackers, and herbivores may induce counterdefenses that Fig. 1. Two individuals are dependent on the concentrations of plant of a single clone of the defenses consumed (14–17) (Fig. 4). The Asian and African wa- continuous range of phenotypes induced by ter flea, Daphnia lum- each partner exemplifies a hallmark require- holtzi. The individual ment of the ecological arms race hypothesis on the left was ex- posed to chemical because it allows for escalating phenotypic cues from predaceous change. If these responses are not continuous, fish (induced); the in- then “arms races” in ecological time are less dividual on the right likely. If reciprocal phenotypic change is the was not (control). The result of adaptive plasticity in both partners, sharp helmet and ex- then it is predicted that coevolution may re- tended tail spine of the induced morph sult in phenotypic plasticity, as opposed to, or protect D. lumholtzi in addition to fixed adaptations. from fish predators. Phenotypic changes in species interac- The uninduced form tions typically revert back to the original was formerly de- phenotypic state after each extended bout of scribed as a different interactions (e.g., each year). However, four species (D. monacha Brehm 1912). Green possibilities
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