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Underappreciated Consequences of Phenotypic Plasticity for Ecological Speciation University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Faculty Publications and Other Works -- Ecology and Evolutionary Biology Ecology and Evolutionary Biology 12-2011 Underappreciated Consequences of Phenotypic Plasticity for Ecological Speciation Benjamin M. Ftizpatrick University of Tennessee - Knoxville Follow this and additional works at: https://trace.tennessee.edu/utk_ecolpubs Part of the Ecology and Evolutionary Biology Commons Recommended Citation International Journal of Ecology Volume 2012 (2012), Article ID 256017, 12 pages http://dx.doi.org/ 10.1155/2012/256017 This Article is brought to you for free and open access by the Ecology and Evolutionary Biology at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Faculty Publications and Other Works -- Ecology and Evolutionary Biology by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. Hindawi Publishing Corporation International Journal of Ecology Volume 2012, Article ID 256017, 12 pages doi:10.1155/2012/256017 Review Article Underappreciated Consequences of Phenotypic Plasticity for Ecological Speciation Benjamin M. Fitzpatrick Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA Correspondence should be addressed to Benjamin M. Fitzpatrick, benfi[email protected] Received 25 July 2011; Revised 22 October 2011; Accepted 12 December 2011 Academic Editor: Andrew Hendry Copyright © 2012 Benjamin M. Fitzpatrick. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Phenotypic plasticity was once seen primarily as a constraint on adaptive evolution or merely a nuisance by geneticists. However, some biologists promote plasticity as a source of novelty and a factor in evolution on par with mutation, drift, gene flow, and selection. These claims are controversial and largely untested, but progress has been made on more modest questions about effects of plasticity on local adaptation (the first component of ecological speciation). Adaptive phenotypic plasticity can be a buffer against divergent selection. It can also facilitate colonization of new niches and rapid divergent evolution. The influence of non- adaptive plasticity has been underappreciated. Non-adaptive plasticity, too can interact with selection to promote or inhibit genetic differentiation. Finally, phenotypic plasticity of reproductive characters might directly influence evolution of reproductive isolation (the second component of ecological speciation). Plasticity can cause assortative mating, but its influence on gene flow ultimately depends on maintenance of environmental similarity between parents and offspring. Examples of plasticity influencing mating and habitat choice suggest that this, too, might be an underappreciated factor in speciation. Plasticity is an important consideration for studies of speciation in nature, and this topic promises fertile ground for integrating developmental biology with ecology and evolution. 1. Introduction of speciation” [13–15]isaspecialcaseofecologicalspecia- tion, and I review the subject by breaking down the effects Phenotypic plasticity has often been seen primarily as an of plasticity on the two components of ecological speciation: alternative to genetic divergence and a feature making popu- adaptive divergence and the evolution of reproductive isola- lations less responsive to natural selection [1–3]. For exam- tion [28]. I close with a few suggestions for future work. ple, those studying adaptation and speciation have often used By any definition, speciation requires genetic divergence. phrases like “merely plastic” to contrast environmentally Therefore, integration of ecological developmental biology ff induced variation against geographic or species di erences with the well-developed body of fact and theory on the with strong genetic bases [4–8]. However, others suggested genetics of speciation [29–31]willbemoreproductivethan that phenotypically plastic traits can promote adaptive evo- attempting to replace this population genetic foundation. lution and the origin of species [9–16]. The general issue of Recent reviews and models support this perspective [27, 32– plasticity and adaptation has been reviewed extensively in the 37]. last decade (e.g., [15, 17–26]). Adaptive plasticity’s impact on speciation was recently reviewed by Pfennig et al. [27], and I do not attempt to duplicate their efforts. Instead I make a few 2. Definitions points that have not been emphasized in the recent literature. In particular, nonadaptive plasticity and environmentally Understanding the relationship between environmental induced barriers to gene flow deserve greater attention. induction and speciation requires a set of consistent def- After making explicit my working definitions of key initions. Terms like “environment,” “speciation,” “plastic- terms, I argue that the “developmental plasticity hypothesis ity,” and “natural selection” are sometimes assumed by 2 International Journal of Ecology different workers to have different definitions, and this can To put it another way, natural selection exists whenever affect communication [38]. The definitions that follow are phenotypic variation causes covariance between phenotype intended to clarify what I mean by certain words and phrases and fitness [43, 44]. Fitness is metaphorical shorthand for within this paper; they are not intended to challenge or the ability to survive and reproduce. It is important to replace alternative definitions. I believe I have followed recent emphasize that natural selection, under this definition, can convention in all cases [39, 40]. exist without genetic variation and can recur over many generations without causing evolution [15, 17]. Adaptation. Genetic change in response to natural selection and resulting in organisms with improved performance with Plasticity. The ability of a single genotype to express different respect to some function or feature of the environment. phenotypic values or states under different environmental conditions, that is, in response to environmental induction. Countergradient Variation. Pattern of geographic variation Plasticity can include developmental plasticity, physiological in which genetic differences between populations affect acclimation, or behavioral flexibility. Plasticity might be their phenotypes in the opposite way from environmental adaptive or not. Adaptive plasticity is a tendency for a differences between populations. For example, if the mean genotype to express a phenotype that enhances its ability phenotype of population i is given by the sum of genetic to survive and reproduce in each environment. Nonadaptive and environmental effects Pi = Gi + Ei, and the effect of plasticity includes any response to environmental induc- environment 2 tends to increase the phenotypic value relative tion that does not enhance fitness (including maladaptive ff to environment 1 (E2 >E1), countergradient variation would responses). Noisy plasticity is e ectively unpredictable phe- exist if G2 <G1. Without genetic differentiation the expected notypic variation owing, for example, to developmental difference in phenotype would be P2 − P1 = E2 − E1,but instability or random perturbations within environments countergradient variation reduces that difference and might [45]. Phenotypic plasticity and environmental induction are even make P2 <P1. More formally, countergradient variation twin concepts; plasticity emphasizes an organismal property is negative covariance between genetic and environmental (the propensity to express different phenotypes in different effects on phenotype [41]. environments), and environmental induction emphasizes the action of the environment. Phenotypic plasticity might Environment. Here, I consider environment to include any- exist even in a homogeneous population in a homogeneous thing external to a given individual organism. Environment environment. Environmental induction happens when envi- includes other organisms (siblings, mates, competitors, ronmental heterogeneity causes phenotypic heterogeneity. predators, prey, etc.) in addition to the physical and chemical surroundings. Given this definition, different individuals in Polyphenism. Expression of more than one discrete pheno- the same place might experience different environments. typic state (alternative phenotypes) by a single genotype (a Neither ecological speciation nor environmentally induced special case of phenotypic plasticity). variation require environmental differences to be associated ff with geography. To put it another way, the e ects of environ- Reaction Norm [or Norm of Reaction]. The set of expected ff ment on fitness and on development might di er among co- phenotypic states or values expressed by a genotype over a occurring individuals for a variety of reasons, often involving range of environments. feedbacks between phenotype and environment [42]. For example, small tadpoles in a pond might experience food Speciation. Speciation is any process in which an ancestral shortages or attacks from predators while large tadpoles in species gives rise to two or more distinct descendant species. the same pond have access to more food and experience less There is some disagreement about whether “speciation” predation (or a different set of predators). should be synonymous with the evolution of reproductive
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