Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation.

SPECIAL SECTION doi:10.1111/evo.12348

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION Carl D. Schlichting1,2,∗ and Matthew A. Wund3,∗ 1

Department of Ecology & Evolutionary Biology, U-3043, University of Connecticut, Storrs, Connecticut 06269 2

3

E-mail: [email protected]

Department of Biology, The College of New Jersey, PO Box 7718, Ewing, New Jersey

Received October 17, 2013 Accepted December 22, 2013 The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation. KEY WORDS:

Adaptive evolution, DNA methylation, epigenetic marking, genetic accommodation, genetic assimilation,

phenotypic plasticity.

There has been growing interest in the importance of modes of evolutionary change that incorporate phenotypic plasticity or epigenetic inheritance. Both conceptual and mathematical models conclude that the incorporation of such “developmental” effects produces key features that set them apart from standard modes of evolutionary change: (1) the potential for temporally decoupling the two phases of adaptation by natural selection (phenotypic selection and genetic response), and (2) the capacity to significantly alter the evolutionary dynamics followed by populations. Plasticity and epigenetic modification share the distinction of causing changes in phenotype or gene expression without changes in DNA sequence. Drawing a bright line between them is becoming increasingly difficult (Grativol et al. 2012): many epigenetic marks are environmentally induced, plasticity itself can be mediated by ∗ These

authors contributed equally to this work. C

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epigenetic modification, and transgenerational (maternal) effects may be due to maternal plasticity (e.g., provisioning) or to epigenetic inheritance. The ecological importance of phenotypic plasticity has long been recognized as a means of adaptively modifying the phenotype in response to environmental change (Sultan 1995; Miner et al. 2005). Scenarios advocating an evolutionary role were first proposed in the late 19th century (organic selection and the Baldwin effect: Baldwin 1896a, b; Morgan 1896; Osborn 1897), and again, independently, in the mid-20th century by C. H. Waddington (genetic assimilation: Waddington 1957) and I. I. Schmalhausen (stabilizing selection: Schmalhausen 1949). Table 1 provides definitions of these and other terms used in this article (for reviews see Schlichting and Pigliucci 1998; Robinson and Dukas 1999; Braendle and Flatt 2006; Crispo 2007). Recent conceptual development also supports a broadened role for

C 2014 The Society for the Study of Evolution. 2014 The Author(s). Evolution Evolution 68-3: 656–672

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Table 1.

Definitions of terms used in this article.

Baldwin effect—In this plasticity enhances the survival of an individual in a new environment; subsequent (organic) selection favors heritable variation in the direction of the plastic response, with a focus on changes in trait means (see Crispo 2007 for elaboration). Chromatin remodeling—Chromatin remodeling refers to changes to chromatin structure via changes to histones or nucleosomes, resulting in changes in gene expression. Cryptic genetic variation—This genetic variation is revealed by environmental or genetic perturbations (Gibson and Dworkin 2004). Epialleles—These are alternative methylation or chromatin states at a given locus (Johannes et al. 2009). Epigenetic effect—“A stably heritable phenotype resulting from changes in a chromosome without alternations in the DNA sequence” (Berger et al. 2009). Epigenetic inheritance—“The stable inheritance of epigenetic marks across multiple generations” (Smith and Ritchie 2013). Epigenetic mark— Epigenetic marks are chemical modifications to DNA, RNA, or proteins that influence chromatin state and gene expression (Smith and Ritchie 2013) including methylation, protein modifications (e.g., acetylation, deacetylation, ubiquitination, and histone methylation), and RNA-based regulatory systems (e.g., small and large noncoding RNAs). Genetic accommodation (s.s.)—It is a process by which phenotypic variants that are initially strictly environmentally induced are selected to become genetically determined (i.e., heritable) (see West-Eberhard 2005a; Crispo 2007). Genetic assimilation—It is a process by which a character state, produced initially by means of a plastic response, is subsequently fixed due to genetic modifications via selection that favors the loss of plasticity (Robinson and Dukas 1999; Pigliucci and Murren 2003). It is a type of genetic accommodation. Cases of loss of plasticity are regularly categorized as assimilation even in the absence of evidence of selection, and some of these are likely due to relaxed selection and drift. Genetic compensation—It is selection for similar phenotypes in different environments, achieved by divergence in underlying physiological plasticity. It can produce countergradient variation (i.e., where selection favors trait values in a direction opposing plastic response; Grether 2005). A type of genetic accommodation. Methylation—It is addition of a methyl group to a cytosine or adenine DNA nucleotide; methylation blocks access to DNA by transcriptional machinery and inhibits gene expression. Phenotypic accommodation—“Adaptive mutual adjustment, without genetic change, among variable aspects of the phenotype, following a novel or unusual input during development” (West-Eberhard 2005b). Inputs can be genetic or environmental. Phenotypic plasticity—“Any change in an organism’s characteristics in response to an environmental signal” (Schlichting and Smith 2002). Small RNAs—Micro-RNAs (miRNAs) are short RNA molecules that bind with complementary mRNAs and block translation. Small interfering RNAs (siRNAs) are short double-stranded RNA molecules that operate in RNA interference, blocking expression of genes that contain complementary sequences. Stabilizing selection (sensu Schmalhausen)—It is environmental change that elicits a hidden portion of the reaction norm, with selection then favoring mutations that enhance responses to the environmental factor; finally, selection ultimately favors a stabilization of the reaction norm. Schmalhausen envisioned an evolutionary transition from simple passive responses to responses controlled by regulatory systems that might ultimately even anticipate environmental change. phenotypic plasticity in evolutionary processes because it mediates the relationship between genotype (which is inherited) and phenotype (the target of selection) by altering gene expression, trait development, and phenotypic integration (Rollo 1994; Schlichting and Pigliucci 1998; Price et al. 2003; West-Eberhard 2003; Schlichting 2004; Ghalambor et al. 2007; Pfennig et al. 2010; Moczek et al. 2011; Thibert-Plante and Hendry 2011; Fitzpatrick 2012; Wund 2012). Such alterations not only modify the strength of selection on the phenotypes and forestall the necessity of genetic change, but also direct the outcome of evolution by determining the availability of phenotypic variants. In this article we focus on genetic accommodation (WestEberhard 2003), a process (1) initiated by phenotypic responses to environmental stimuli enabling population persistence, and (2)

followed by genetic changes that enhance their adaptive value. A new phenotypic variant is genetically “accommodated” (i.e., its reaction norm evolves) through selection on genetic variation for altered patterns of gene expression and their associated phenotypic effects, leading to increased frequency of that phenotype. Genetic accommodation may take several forms: loss of or decreased plasticity (e.g., genetic assimilation), enhanced or altered plasticity, or selection for similar phenotypes in different environments (e.g., genetic compensation). Such changes are not isolated to the trait of interest, but may also extend to changes in the relationship of the trait to other aspects of the phenotype over the course of the organism’s ontogeny, that is, accommodation can also involve modifications of aspects of the phenotypic and genetic architecture of trait interrelationships.

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In this article we briefly examine evolutionary models that explicitly incorporate plastic/epigenetic developmental variation, and review studies that investigate (1) the mechanisms of phenotypic plasticity and (2) the environmental sensitivity of epigenetic modification. We assess the strength of empirical evidence for roles of phenotypic plasticity and epigenetic inheritance in facilitating evolutionary change, and present a diversity of empirical and model-based evidence for plasticity’s impacts on evolutionary processes.

An Example of Genetic Accommodation in Humans: The Evolution of Hypoxia Tolerance Before an extensive review of mechanisms and evidence, we wish to clarify our perspective by taking a familiar example of adaptation to extreme conditions, hypoxia tolerance, and view it through the lens of genetic accommodation. Lowland-inhabiting humans exhibit a suite of plastic responses upon ascent to high altitude: rapid increases in breathing rate (hyperventilation with concomitant alkalosis) and heart rate, followed by suppression of other functions (e.g., digestion) and decreased plasma volume. Subsequent acclimatization results in increased production of erythrocytes, capillaries, mitochondria, and aerobic enzymes, and reduced stroke volume. These responses to hypoxia are mediated by the hypoxia-inducible factor (HIF) signaling cascade, which affects expression of genes involved in erythrocyte production, glycolysis, pH homeostasis, lipid metabolism, and the formation of new blood vessels (Chen et al. 2012a; Keith et al. 2012). Human populations adapted to high altitude have genetic features that are related to the adaptive plastic responses of lowland populations. Tibetans inhale more air with each breath, breathe more rapidly, and have higher cerebral blood flow, but have significantly lower oxygen saturation. Andeans have oxygen saturation levels and breathing rates similar to lowland populations, but have increased oxygen carrying capacity/red blood cell. Amhara Ethiopians have little reduction in oxygen saturation or increase in hemoglobin levels, whereas Oromo Ethiopians have reduced oxygen saturation and increased hemoglobin levels (Beall et al. 2002; Beall 2006; Alkorta-Aranburu et al. 2012). These different patterns suggest convergent evolution for hypoxia tolerance, an inference strengthened by the results of genetic analyses. Significant progress has been made in understanding genetic bases for these adaptations, including evidence for significant natural selection at some loci. Two HIF pathway loci, EGLN1 (HIF-1 pathway) and EPAS1 (HIF-2α), are associated with reduced hemoglobin levels, although the alleles differ between populations (Bigham et al. 2010; Simonson et al. 2010; Yi

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et al. 2010; Xu et al. 2011). Variants of EGLN1, which degrades HIF under normal conditions, are under positive selection in both Tibetan and Andean samples, whereas Tibetan EPAS1 is under very strong selection (Bigham et al. 2010; Yi et al. 2010; Xiang et al. 2013). Other candidate genes in the HIF pathway have been identified—PPARA, a transcription factor regulating lipid metabolism, is under selection in Tibet (Simonson et al. 2010; Ge et al. 2012) and THRB and ARNT2 are under selection in Ethiopia (Scheinfeldt et al. 2012). A strong signal of selection in Ethiopian populations has also been found for BHLHE41, a hypoxia-inducible transcription repressor (Huerta-Sanchez et al. 2013). These evolutionary changes in genes in the ancestral HIF pathway suggest genetic accommodation via mutations in genes regulating expression of plastic responses to hypoxia (such as EGLN1 and HIF1AN), perhaps through constitutive production of HIFs. Similarly, a loss of function of EPAS1, involved in hypoxia-related increased erythrocyte production, could reduce the plastic response to low oxygen and produce the characteristic low hemoglobin concentrations of Tibetans.

Models of How Plasticity Mediates Evolutionary Response Models of the effects of plasticity on evolutionary change have emphasized the distinct nature of the evolutionary process when plasticity is included in addition to the traditional mode of allelic substitution. Chevin and Lande have modeled the role of plasticity in mitigating various pressures on populations due to changes in environmental conditions. Lande (2009) examined plasticity’s facilitation of the evolutionary response to a novel environment through initial evolution of adaptive plasticity followed by fixation of a new phenotypic optimum. Chevin et al. (Chevin and Lande 2010; Chevin et al. 2010) demonstrated that plasticity plays a role in population persistence by blunting the effective size of the environmental change and subsequently increasing the rate of adaptation. In a marginal environment, plasticity can ameliorate the effects of the flow of maladaptive alleles from central populations by raising fitness and, concomitantly, overall population size (Chevin and Lande 2011). Frank (2011) summarized a variety of models of how plasticity/learning can play a significant role in adaptation in the absence or presence of genetic variation. His fundamental conclusion was that plasticity’s ability to smooth a fitness landscape by producing phenotypes that are viable and thus promote population persistence, changes “evolutionary dynamics in a way that greatly accelerates adaptation to novel or extreme environmental challenges” (see also Hinton and Nowlan 1987; Ancel 2000; Saito

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et al. 2013). Such benefits accrue even when phenotypic plasticity is random with respect to the optimum phenotype. Although random phenotypic response can lead to high “search costs” (Frank 2011; Saito et al. 2013), such effects can be avoided when plastic responses begin in the vicinity of genetic variants or when plasticity is biased in the direction of the phenotypic optimum. Results of models of the evolutionary effects of epigenetic transmission mirror those for phenotypic plasticity in demonstrating a decoupling of phenotypic selection from genetic responses (Day and Bonduriansky 2011; Klironomos et al. 2013). These models also show complex evolutionary dynamics when both genetic and epigenetic inheritance are permitted (Bonduriansky and Day 2009; Geoghegan and Spencer 2012; see Furrow and Feldman 2014 for an in-depth review). An additional effect on evolutionary rate is plasticity’s potential to permit the accumulation of genetic variation, variation that can subsequently be released in response to genetic or environmental stress. Exposing such cryptic genetic variation may have significant effects on the evolutionary trajectories of populations (Gibson and Dworkin 2004; Dworkin 2005a; Flatt 2005; Moczek 2007; Le Rouzic and Carlborg 2008; Schlichting 2008; McGuigan and Sgrò 2009; Masel and Trotter 2010; Draghi and Whitlock 2012; Iwasaki et al. 2013).

Genetic Mechanisms Underlying Phenotypic Plasticity Microarray studies made it abundantly clear that expression patterns of hundreds or thousands of genes can be altered by various environmental challenges (e.g., Gasch et al. 2000; Colbourne et al. 2011; and see Kilian et al. 2012 for a synthesis of data from plant studies). Because microarray results are strictly correlative, further studies were instigated to examine likely candidates for environment-dependent up- or downregulation (e.g., Rabbani et al. 2003; Larsen et al. 2008; Coolon et al. 2009; Spanier et al. 2010). Such studies have now largely given way to transcriptomic investigations of plasticity (Gracey et al. 2004; Cheviron et al. 2008; Chapman et al. 2011; Zhou et al. 2012). These genomic approaches have been reviewed by AubinHorth and Renn (2009). They emphasize three foci: (1) What is the genomic signature of plasticity? In a genomic reaction norm, what genes are responsive, and when during the development of the plastic traits are they responsive to particular environments? (2) What biological pathways are employed in plastic responses? Can modules of genes be identified that underly responses to particular stimuli? and (3) what are the mechanisms transducing environmental signals? Their review highlights studies addressing the first two of these, mostly for animal systems (for gene regulation in plants see Chen et al. 2012b; Luo et al. 2012; Mizoi

et al. 2012; Nakashima et al. 2012; Puranik et al. 2012; Scharf et al. 2012; Yang et al. 2012; for environmental sensing in plants see Osakabe et al. 2013). Roelofs et al. (2010) reviewed evidence for transcriptional plasticity, and collated evidence suggesting that evolution in response to severe stress (e.g., DDT, heavy metals) may favor constitutive overexpression of some genes. Beldade et al. (2011) provide a brief review of molecular mechanisms of plasticity in the context of a broader overview of the evolution of adaptive plasticity of animal morphology. All these reviews indicate that this field is still in its infancy—few studies reach what we would consider the “gold standard” of integrating developmental and comparative approaches (Hodgins-Davis and Townsend 2009; Whitehead 2012): a minimum of three environments, several developmental stages, and comparisons of closely related taxa (ecotypes or species). Several recent studies give a flavor for the current work on plasticity of gene expression. Le Trionnaire et al. (2012) obtained transcriptomic profiles for pea aphids in summer versus autumn conditions to examine the shift in reproductive mode in response to photoperiod. They found 367 differentially expressed transcripts, specifically those involved in juvenile hormone (JH) production and signaling. Tine et al. (2012) compared six populations of the black-chinned tilapia, Sarotherodon melanotheron, from salinities ranging from 0 (fresh water) to 100 ppt (hypersaline). Focusing on differential expression of 11 genes responsive to salinity differences, their qRT-PCR results identified two groups based on mRNA levels: a group they refer to as trade-off genes that had high versus low expression for populations at opposite salinity extremes, and stress genes that showed low expression in fish from intermediate salinities, but high expression in fresh and hypersaline populations. Whitehead et al. (2011) contrasted populations of killifish (Fundulus) from different salinity regimes (fresh, brackish, and salt) that also represented distinct points on an allele frequency cline. Fish acclimated to seawater were challenged with brackish/fresh water in the laboratory, and gene expression measured at six time points. They characterized four sets of environmentresponsive genes and categorized many genes to functional (ontology) groups. Genes whose patterns of expression changed over time represent a core acclimation set shared among populations. A second set comprises genes with population-specific expression levels, but that do not differ in time course; two-thirds of these genes differed in a manner that suggested local adaptation of the freshwater population. The third set of genes had shared time-dependent expression patterns but population-specific expression levels: nearly all distinguished the freshwater from the brackish/saline populations. Finally, genes whose time-dependent expression patterns differed among populations, that is, genes whose plastic responses to salinity differed over time and among populations, showed greatest divergence among populations at


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the earliest time points after the hypo-osmotic shock. These patterns provide strong support for a scenario of local adaptation to freshwater. The authors suggest that the pattern of adaptive differentiation in this system indicates that genes with plastic expression profiles are more likely to be targets of selection (see also Hunt et al. 2013). Although our knowledge of the mechanisms of plastic response are increasing, to date there are few studies that link mechanisms of plasticity with particular patterns of genetic accommodation. Renn and Schumer (2013, Fig. 2) proposed a set of patterns of gene regulatory change expected for different scenarios of genetic accommodation. Loss-of-function of genes that result in constitutive expression of what was initially a plastic response is a clear candidate for cases of the loss of plasticity (e.g., genetic assimilation via selection or drift). Likewise, changes in patterns of regulation of specific genes are likely candidates to provide adaptation to particular local environmental regimes (Schwartz et al. 2009). Unfortunately, even in the best-studied systems (e.g., Arabidopsis flowering time), there are still too few studies that link regulation of specific genes with particular plastic responses. We are just beginning to decipher the actions of individual transcription factors—which may bind to hundreds of genes across a genome—or unravel the extraordinarily complex gene regulatory networks in which they operate (Yant 2012). At this time only a few studies have deciphered the genetic basis of genetic accommodation (see below), far too few to draw general conclusions about its genetic architecture. ENVIRONMENTAL EFFECTS ON EPIGENETIC MARKING

The results of many studies investigating the role of DNA methylation in plasticity remain largely correlative, that is, differences in methylation are associated with environmental gradients or treatments (see, e.g., Bossdorf et al. 2010; Mishra et al. 2011; Herrera et al. 2012; Massicotte and Angers 2012; Richards et al. 2012; Smith et al. 2012; Flores et al. 2013; Herrera and Bazaga 2013; Zhang et al. 2013). Only rarely have loci been identified whose methylation could explain the phenotypic changes (e.g., Waterland et al. 2007). Weiner and Toth (2012) reviewed evidence for the role of methylation in caste determination in social insects. Holeski (2007) found that Mimulus guttatus plants that were induced to produce more trichomes in response to herbivory also produced offspring with elevated trichome levels even if offspring were not damaged. Scoville et al. (2011) also studied Mimulus trichome production, investigating the role of epigenetic marking. They found that MYB MIXTA-like 8 expression was negatively correlated with trichome production, and was significantly downregulated in both damaged parental leaves and in undamaged progeny, suggesting that downregulation was transmitted epigenetically to offspring.

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The jasmonic acid (JA) signaling cascade is responsible for triggering production of defensive compounds in response to herbivory. Rasmann et al. (2012) examined how herbivory on maternal Arabidopsis plants affected several generations of offspring, examining effects on defensive compound production, herbivore performance and gene expression. CORONATINE INSENSITIVE1 (COI1) mediates degradation of a key inhibitor of the JA pathway allowing transcription of the genes for defensive compounds. A segregating population of COI1/coi1–1, COI1/COI1, and coi1–1/coi1–1 plants was produced and half the parents were subjected to herbivory by Pieris rapae; caterpillar growth and JA-induced gene expression were measured on offspring plants. Caterpillars fed offspring of coi1–1/coi1–1 plants did not differ in mass whether parent plants were damaged or not; caterpillars fed offspring of COI1/– plants were significantly smaller if the parent plants had been damaged, even those caterpillars fed on coi1–1/coi1–1 progeny. Two genes in the JA pathway, LOX2 and AOS, were expressed more strongly in plants whose parents had been damaged. In addition, Arabidopsis lines deficient in short interfering RNA (siRNA) synthesis and processing did not inherit resistance from damaged parents (Rasmann et al. 2012). These few studies offer a glimpse into mechanisms of environmentally dependent epigenetic modification, but the evolutionary implications are rudimentary at best and substantial further work is necessary (Grativol et al. 2012).

Evidence for Genetic Accommodation Here we evaluate evidence for genetic accommodation as a means of gauging its plausibility as an alternative evolutionary pathway. We are not testing hypotheses about the relative frequencies of accommodation and allelic substitution. Despite the likely transient nature of genetic accommodation (Pigliucci and Murren 2003), there are a number of circumstances in which its role can be discerned (reviewed in Wund 2012). Our classification scheme (Fig. 1, Tables S1A and B) distinguishes categories of evidence in a qualitative fashion (complete results in Table S2). Our survey aims to be comprehensive, not exhaustive, appraising the scope and strength of evidence in each study. Wund (2012) reviewed some of the same literature with the goal of outlining approaches to testing relevant hypotheses, not to review the strength of the evidence. Figure 1 is organized based upon the nature of the evidence, and whether that evidence involves direct documentation of a specific process, or an indirect inference based upon either phylogenetic comparisons or plausibility arguments. Although experimental evolution studies provide definitive evidence for demonstrating both the possibility and mechanisms of genetic accommodation, evidence from natural populations is

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Figure 1.

Histogram showing studies that provide evidence for genetic accommodation, or that are suggestive of the importance of

plasticity as a facilitator of evolution. Papers were subdivided based upon the nature of evidence they present (black bars: ancestordescendant comparisons; lined bars: experimental evolution; gray bars: phylogenetic inference; cross-hatched bars: genetic accommodation is plausible, but not demonstrated). Bars show the number of papers assigned to each category. Numbers above the bars indicate the number of taxa investigated by the papers within that category. References and taxonomic groups are listed in Table S2.

preferable for indicating the relevance of this process in nature. The most direct evidence from natural systems comes from cases where reaction norms from ancestral and derived (or sister taxa) can be directly compared to determine whether trait means or their plasticities have adaptively diverged: mainland-island pairs, populations with recent range expansions, or species that accumulate a bank of developmentally arrested offspring, allowing “resurrection” studies to contrast individuals from before and after an environmental change. When ancestors and descendants cannot be evaluated directly, phylogenetic inferences can allow the indirect assessment of genetic accommodation by relating patterns of plasticity within taxa to adaptive differences among taxa. Our final column in Table S1 comprises plausible cases based upon the presence of adaptive plasticity and its possible link to adaptive evolution; these require further investigation. EVIDENCE FOR PLASTICITY AS A PRECURSOR TO PHENOTYPIC EVOLUTION

When environments change, phenotypic plasticity can stimulate evolution, either by permitting survival under novel selection pressures, and/or by revealing previously cryptic genetic variation. By establishing the initial distribution of phenotypes available to selection, the nature of plastic responses can influence

the outcome of genetic evolution. Abundant evidence supports the hypothesis that adaptive plasticity can allow populations to cope with environmental change (Table S2). It is not surprising that many examples emerge from human-altered systems, where novel environments, and adaptively plastic responses to them, are common (Hendry et al. 2008): individuals of some species have adaptively adjusted their breeding cycles in response to climate change (Reale et al. 2003) or their mating behavior in response to eutrophication in aquatic habitats (Candolin 2009). Biological invasions also offer windows into how populations respond developmentally and evolutionarily to novel environments. The rapid range expansion of house finches (Carpodacus mexicanus) throughout North America has been facilitated by integrated physiological, morphological, and behavioral plasticity in response to temperature variation. These changes have led to adaptive maternal effects that impact both phenotypic variance and offspring fitness, which shape the course of genetic evolution in newly established populations (Badyaev 2009). Similarly, the colonization of a coastal, Mediterranean environment by darkeyed juncos (Junco hyemalis) from a higher elevation, temperate region was facilitated by plasticity of breeding cycles (Yeh and Price 2004). These changes in turn led to altered patterns of sexual selection on plumage coloration (Price et al. 2008), exemplifying


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how plasticity in one aspect of the phenotype can alter the evolutionary trajectory of correlated traits. Plastic increases in plant height and leaf area in response to shading have permitted the successful invasion of forests by the perennial herb Prunella vulgaris, leading to genetic assimilation—formerly plastic responses are now constitutively expressed in the invasive population (Godoy et al. 2011). In an ancestral environment, selection can act to canalize the expression of genetic variation, such that a variety of genotypes produce similar, selectively equivalent phenotypes (Mather 1942; Waddington 1942; Muller 1949; Hermisson and Wagner 2004; Félix and Wagner 2008; Le Rouzic and Carlborg 2008). When conditions change, this cryptic genetic diversity can be expressed, immediately altering the distribution of the heritable phenotypic variation available to selection (Gibson and Dworkin 2004; Le Rouzic and Carlborg 2008; Schlichting 2008; McGuigan and Sgrò 2009). A variety of “capacitors” have been identified (Tirosh et al. 2010; Ruden 2011; Takahashi 2013), for example, chaperonins such as HSP90—under typical conditions these help protein products of alternate alleles fold in similar ways; under stressful conditions, such mechanisms can break down and reveal underlying genetic variation (Rutherford and Lindquist 1998; Queitsch et al. 2002; Gibert et al. 2007; Sangster et al. 2008; Lindquist 2009). Much of the evidence that environmental perturbations can reveal cryptic genetic variation (Table S2) stems from studies of traditional model organisms such as Drosophila (e.g., Dworkin 2005b; Debat et al. 2009; Takahashi 2013), but it has also been documented in studies of adaptation to natural environments (Ledon-Rettig et al. 2010; McGuigan et al. 2011). Rohner et al. (2013) found that HSP90 acts as a “capacitor” for populations of surface-dwelling Astyanax mexicanus, exposing variation that can be selected to produce smaller eyes. In addition they showed that, when raised in water with low conductivity characteristic of cave environments, surface fish upregulated HSP90 and had significantly increased variation in eye and orbit sizes. They propose that cryptic variation exposed when a surface fish was swept into a cave was selected upon to initiate the loss of eyes in the cave populations (Rohner et al. 2013). Following the production of a novel phenotypic variant, genetic accommodation is the process by which trait form, regulation, expression, associated costs, and integration with other traits evolve (West-Eberhard 2003). The key distinction from the standard model of evolution from genetic variation is that evolutionarily significant phenotypic novelty can arise from environmental or epigenetic alterations of the genotype-to-phenotype map. Table S2 presents a list and classification of potential cases of genetic accommodation. We consider several distinctive forms of genetic accommodation, including evolution of both traits and their plasticities, and describe some examples of what is known about these patterns and their underlying mechanisms.

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DIRECT SELECTION FOR ENHANCED PLASTICITY

It is well established that adaptive phenotypic plasticity can evolve (e.g., Arnqvist and Johansson 1998; Juenger et al. 2000; van Kleunen and Fischer 2001; Baythavong and Stanton 2010; Bento et al. 2010). In cases of the evolution of adaptive plasticity from a less plastic ancestor, enhanced plasticity can evolve as a direct target of selection, rather than as a byproduct of evolution of trait values in a single environment (and concomitant relaxed selection on trait values in the noninducing environment). For example, marine threespine stickleback fish have repeatedly colonized and adapted to diverse freshwater habitats (Bell and Foster 1994). Freshwater populations that exploit a variety of prey exhibit greater plasticity of trophic characters than their planktivorous marine ancestor. Note that this enhanced morphological plasticity is not required for freshwater adaptation in general, because freshwater specialists are not more plastic than marine fish (Svanback and Schluter 2012). The grasshopper Schistocerca emarginata exhibits polyphenic development of aposematic coloration, whereby high population density induces the development of conspicuous coloration. However, not all populations are equally distasteful to predators, and unpalatable grasshopper populations have evolved much greater plasticity in coloration than palatable populations. Sword (2002) argued that this scenario may be common—evolution of aposematism by genetic accommodation via increased plasticity. GENETIC ASSIMILATION

In some cases, plasticity can become reduced or lost—either from selection against costly developmental machinery underlying plasticity or because of relaxed selection when alternative environments are not frequently encountered (Lahti et al. 2009; Maughan et al. 2009; Snell-Rood et al. 2010). Genetic assimilation is the complete loss of plasticity, whereby an environmentally induced trait is selected to become constitutively expressed without the original environmental cue (Pigliucci et al. 2006; Crispo 2007). Waddington’s classic selection experiments involving Drosophila wing venation and bithorax phenotypes (Waddington 1953, 1956) provided the initial empirical evidence for genetic assimilation, with repeated demonstrations in Drosophila (Bateman 1959; Robertson 1964), bacteria (Eldar et al. 2009), mites (Macke et al. 2011), mice (Dun and Fraser 1959), and tobacco hornworm caterpillars (Suzuki and Nijhout 2006). Such selection experiments provide some of the strongest, and most direct evidence of genetic assimilation and accommodation (see below), particularly when molecular mechanisms responsible have been characterized (see Gibson and Hogness 1996; Suzuki and Nijhout 2008a, b; Eldar et al. 2009). Clear cases of genetic assimilation have also been identified under natural circumstances when derived populations exhibit reduced plasticity. A thoroughly investigated case involves the loss

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of head size plasticity in Australian tiger snakes (Neotechis scutatus). Mainland snakes have established populations on numerous islands off the southern Australian coast, where they ingest considerably larger prey. Mainland snakes fed large prey exhibit little or no plasticity of head size, whereas snakes from a recently established (90 years) island population do, suggesting rapid evolution of an adaptively plastic response (Aubret 2004). Longer established island populations show decreasing levels of plasticity of jaw length, consistent with genetic assimilation (Aubret and Shine 2009): development of larger jaws leads to decreased overall growth rates and a lag time for optimal jaw size production, suggesting selection to eliminate costs associated with plasticity (Aubret and Shine 2010). Range expansions are often informative, because individuals at range margins often are near physiological limits, leading to the expression of novel phenotypic variants. For example, some individuals of the lycaenid butterfly (Zizeeria maha) express modified color patterns in response to cold shock at the edge of their range, responses that appear to have become partially assimilated. Assimilation of these color patterns was subsequently recapitulated in a selection experiment starting with wild-caught stock (Otaki et al. 2010). When direct comparisons with ancestors are not possible, phylogenetic inferences can reveal instances of genetic assimilation when plasticity represents a primitive condition and constitutive expression is derived. In reptiles, genotypic sex determination has evolved numerous times from temperature-dependent sex determination (Janzen and Paukstis 1991), indicating repeated cases of genetic assimilation. King crabs (Lithodidae), shell-less and bilaterally symmetric, have evolved from shell-bearing, highly asymmetric ancestors (Tsang et al. 2011). In a sister clade with innate asymmetry, one species of hermit crab (Clibanarius vittatus) has been shown to become symmetric following successive molts if shells are not provided (Harvey 1998). The implication is that loss of the shell in the ancestor of king crabs involved an initial plastic switch to bilateral symmetry that was subsequently genetically assimilated into a fixed developmental pattern. This scenario is an excellent example of how environmental impacts on development (in this case, the absence of a gastropod shell) can initiate new trajectories of phenotypic evolution. GENETIC COMPENSATION

When populations of the same species inhabit different environments, divergent selection may lead to divergent norms of reaction among those populations. This scenario is a multipopulation extension of the general processes involved in genetic accommodation described above. In some cases, norms of reaction differ among populations because selection favors the production of similar phenotypes in different environments. Such genetic compensation involves the evolution of plasticity to limit phenotypic

differences among individuals along an environmental gradient (Grether 2005), resulting in a pattern of countergradient variation (Conover and Schultz 1995; Conover et al. 2009). Few examples of genetic compensation exist (reviewed in Grether 2013), and it is unclear whether the paucity of evidence results from rarity or that its discovery requires investigation of whether populations that are phenotypically similar under natural conditions differ under common experimental conditions. Good examples of genetic compensation include the convergence of sexual coloration in guppies (Poecilia reticulata) along a gradient in dietary carotenoids (Grether et al. 2005; Deere et al. 2012) or convergence in antipredator adaptations in Daphnia populations that experience different predation regimes (Dennis et al. 2011). GENERAL CASES OF GENETIC ACCOMMODATION

Ample empirical evidence exists demonstrating more general patterns of genetic accommodation, in which changes in reaction norms evolve as byproducts of selection for new phenotypic optima, but in which plasticity is neither lost completely (assimilation), nor is it necessarily the direct target of selection. Here we briefly describe several compelling cases, representing a diversity of empirical approaches. The polyphagous aphid Aphis fabae uses many different host plants, aided by phenotypic plasticity. Gorur et al. (2005) selected for use of a novel host, and demonstrated that phenotypic plasticity of life-history traits enabled initial success, and that these plastic reaction norms evolved over successive generations to improve fitness. Parasitism in nematodes has evolved numerous times, perhaps facilitated by the their ability to express a developmentally arrested “dauer” phenotype in response to stress. Stasiuk et al. (2012) found that a facultatively parasitic species, Parastrongyloides trichosuri, uses the developmental mechanisms responsible for dauer formation to switch from a free-living to parasitic life history. Furthermore, they successfully up- and downselected the threshold for responses to the environmental cue, demonstrating the ease of achieving genetic accommodation in this system. Each of these cases involve evolution from standing variation in reaction norms, with plasticity facilitating particular evolutionary outcomes that correspond to the nature of the plastic responses themselves. When ancestral and derived populations can be directly compared, many potential examples are observed of genetic accommodation playing a role in adaptive evolution. The threespine stickleback (Gasterosteus aculeatus) is a model for the study of behavior and evolution because diverse freshwater populations can be directly compared to oceanic progenitors (Bell et al. 2004; Gelmond et al. 2009). Genetic accommodation has likely played a role in morphological (Wund et al. 2008; Spoljaric and Reimchen 2011; Svanback and Schluter 2012; Wund et al. 2012), behavioral (Shaw et al. 2007), and osmoregulatory (McCairns and Bernatchez 2010) adaptation to freshwater environments.


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Human-facilitated invasions can also catch genetic accommodation in the act. For example, common ragweed (Ambrosia artemisiifolia) is native to North America and invasive in Europe. Reaction norms for growth rate and reproductive success have adaptively diverged in the introduced populations (Hodgins and Rieseberg 2011), and these appear related to divergent patterns of gene expression (Hodgins et al. 2013). Scoville and Pfrender (2010) compared pigmentation of Daphnia in lakes with and without salmonid predators, elucidating several different manifestations of genetic accommodation. In fishless lakes, Daphnia melanin production is a plastic response to UV exposure mediated by plastic downexpression of dopa decarboxylase (Ddc); the pigmentation gene ebony is transcribed at low levels. In lakes with fish, neither melanin nor Ddc production is plastic; these lakes have a higher constitutive production of ebony. Thus, genetic accommodation has facilitated the evolution of cryptic coloration in lakes experiencing selection by recently introduced predators, through both genetic assimilation and shifts in mean expression of genes underlying melanin production. A particularly thorough set of experiments have demonstrated that the repeated colonization of freshwater by the marine copepod Eurytemora affinis has been facilitated by genetic accommodation of Na+ /K+ and V-type H+ ATPase activity (Lee 1999; Lee and Petersen 2002; Lee et al. 2011). These evolutionary modifications were observed in multiple freshwater populations and in multiple lines selected in the laboratory (Lee et al. 2011). Some species produce embryos or seeds that can remain dormant for many years, potentially spanning changes in the environment. Patterns of plasticity of offspring from different generations can be compared in “resurrection” experiments (reviewed in Hairston and De Meester 2008) to evaluate evolutionary responses. This approach has been used to document genetic accommodation in Daphnia physiology and behavior in response to both eutrophication and predator introductions (Hairston and De Meester 2008). Plants are especially amenable to resurrection studies. Polygonum cespitosum, an annual plant native to Asia with a persistent seed bank, is invasive in North America. A resurrection study has demonstrated that in only 11 years, an invasive population has evolved to tolerate the sunnier conditions in the introduced range, accomplished via the evolution of increased plasticity of root allocation and photosynthetic physiology (Sultan et al. 2013). Phylogenetic inference can be a valuable tool when considering the evolutionary implications of plasticity in driving patterns of macroevolutionary diversification. When patterns of plasticity within a species mirror patterns of phenotypic divergence among species within a lineage, it has been inferred that plasticity drove those patterns of diversification (e.g., Badyaev and Foresman 2000; Gomez-Mestre and Buchholz 2006). An example in the ant genus Pheidole is instructive: a number of species

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express supersoldier castes; these appear to have been lost and regained at least once in the lineage. Supersoldiers can be induced in species where they do not normally occur by the application of JH, revealing a possible mechanism for re-evolution of supersoldiers via genetic accommodation: the ancestral capacity can be reinstated via an alteration in sensitivity to JH during development (Rajakumar et al. 2012). Because of its potential to influence adaptation to divergent conditions, phenotypic plasticity might facilitate speciation by establishing or reinforcing differences among individuals that might become barriers to reproduction (Pfennig and McGee 2010). In periodical cicadas (Magicicada), a plastic shift in the life cycle appears to have led to allochronic speciation (Cooley et al. 2001). Plastic changes in flowering time have been proposed as a general means of initiating reproductive isolation (Levin 2009), with an excellent example in two species of palms on Lord Howe Island, in the South Pacific, where shifts in phenology in response to different soils has facilitated speciation (Savolainen et al. 2006). Similarly, plasticity in niche utilization might also establish or enhance isolation among otherwise compatible individuals. In Arctic charr, Salvelinus alpinus, stable interindividual differences in diet preference and associated morphological plasticity may set the stage for ecological speciation by reinforcing differences in habitat selection (Adams and Huntingford 2002). GENETIC ACCOMMODATION AND PHENOTYPIC INTEGRATION

Regardless of whether heritable variation is present for a focal trait, plasticity in a trait’s form or expression can lead to altered patterns of selection on functionally or developmentally correlated traits for which heritable variation does exist (West-Eberhard 2003, 2005a; Pfennig et al. 2010). Changes in behavior have often been promoted as likely candidates for stimulating the evolution of related morphology and physiology—when organisms adopt a new behavior, such as exploiting a new resource, selection should act on morphology and physiology associated with acquiring and processing those novel resources. Numerous authors have focused specifically on this “behavior first” hypothesis (e.g., Mayr 1958, 1963; Bateson 1988; Wcislo 1989; West-Eberhard 1989), so we will not review the topic further here. Instead, we will focus on identifying additional cases in which a plastic change in one trait directly influences selection on other aspects of the phenotype (Table S2). There is abundant evidence from many organisms that genetic architecture is altered under different environmental conditions (e.g., Donovan and Ehleringer 1994; Czesak and Fox 2003; Messina and Fry 2003; Engqvist 2007; Haugen et al. 2008; Nespolo et al. 2009; Robinson et al. 2009; Sherrard et al. 2009; King et al. 2011), and Falconer (1990) conceptually addressed the

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issue of how selection under different environmental conditions could impact responses (see also Paenke et al. 2007). However, direct evidence whereby an evolutionary response in one trait has been observed to result from a plastic change in another is rare. An exception is a study by van Hinsberg (1998) who selected the plant Plantago lanceolata for long and short leaf lengths under two light regimes—low and high red:far red ratios. Correlated responses to selection depended on the selective environment: for example, plants selected for plastic responses to high red:far red ratios as well as long leaves, had larger seeds and had lower dormancy than those selected for long leaves in low red:far red ratios. Springate et al. (2011) selected for earlier flowering response in Arabidopsis under spring and winter conditions, and found that the initial correlations of flowering time and plasticity (r = −0.9 in spring and r = 0.14 in winter) dictated the outcome of selection—spring conditions selected for increased plasticity, winter for decreased plasticity. To address whether, and how often this phenomenon occurs, we encourage investigators studying genetic accommodation to consider correlated evolution of nonfocal traits. For example, in their investigation of the genetic accommodation of color polyphenism in tobacco hornworms (Manduca sexta), Suzuki and Nijhout (2008a) found that selecting directly for color polyphenism (see above for more detail) resulted in correlated changes in body size. This unintended response to selection arose because both coloration and body size are influenced by a common factor—JH. In the case of the house finch range expansion discussed above, plastic changes in mothers’ reproductive behavior and physiology simultaneously allow them to breed in novel environments while also increasing the production of novel morphological variants in their offspring. This variation in offspring morphology comes under strong selection in the novel environments; thus, plasticity in maternal traits has affected offspring morphology, enabling it to be exposed to selection in novel environments (Badyaev 2009). In general, incubation behavior of oviparous animals is likely to impact the fitness of offspring, and thus alter patterns of selection on both adult life-history and various offspring traits (DuRant et al. 2013).

An Evolutionary Role for Epigenetic Inheritance The literature on environment-dependent epigenetic marking has grown rapidly with a number of reviews highlighting different modes of modification: DNA methylation (Angers et al. 2010; Bonasio et al. 2010; Johnson and Tricker 2010; Faulk and Dolinoy 2011; Grativol et al. 2012; Brautigam et al. 2013); chromatin remodeling (Luo et al. 2012); and miRNAs and siRNAs (see Table 1 for definitions) (Contreras-Cubas et al. 2012; Khraiwesh et al. 2012). Turck and Coupland (2014) provide some examples of

effects of epigenetic marking on plant development and review the mechanistic details of the process of methylation. They suggest that several examples of DNA methylation in plants require the presence of transposons that act to recruit methylation. The evolutionary importance of epigenetic marks has been championed most vigorously by Jablonka and Lamb (Jablonka and Lamb 1995, 1998, 2005; Jablonka 2013), but others have considered this question as well (Kalisz and Purugganan 2004; Rapp and Wendel 2005; Wolf and Hager 2006; Bonduriansky and Day 2009; Gilbert and Epel 2009; Feinberg and Irizarry 2010; Johnson and Tricker 2010; Richards et al. 2010; Shea et al. 2011; Dickins and Rahman 2012; Smith and Ritchie 2013). Data indicate that inheritance of epigenetic marking is extremely common (Jablonka and Raz 2009), and transgenerational plasticity (i.e., maternal effects) has increasingly been implicated in adaptation (Rossiter 1996; Badyaev 2005; Sultan et al. 2009; Holeski et al. 2012). Experimental studies investigating the evolutionary role of epigenetic marking are in their initial stages. Conceptually, there are several key questions regarding the potential evolutionary impact of epigenetic inheritance: (1) How reliable is marking in response to environmental signals? (2) What fraction of marked alleles is transmitted across generations? (3) What is the frequency of resetting of marks—across how many generations can they be transmitted (Becker et al. 2011; Schmitz et al. 2011)? and (4) how much genetic variation is there for epigenetic marking? Results of models of both evolutionary effects of epigenetic transmission and phenotypic plasticity show that decoupling of phenotypic selection from genetic responses results in complex evolutionary dynamics. Although empirical evidence for evolutionary effects of plasticity is plentiful, there is almost none for epigenetics. Nevertheless there are parallels between both the mechanisms of epigenetics and plasticity and their modeled evolutionary outcomes. This suggests that it may be possible to apply insights derived from studying genetic accommodation to understanding the process of evolution of epigenetic modification (Herman et al. 2014). For example, epigenetic markings, if adaptive, could lead to population persistence. Whether these adaptive changes are eventually genetically accommodated will likely depend on the intergenerational stability of the epigenetic modifications. Genetic variation may also be shielded from selection during epigenetic phases, variation that can subsequently be released (Klironomos et al. 2013).

Conclusions There is considerable direct empirical support for most of the proposed processes by which phenotypic plasticity can influence evolutionary trajectories (Fig. 1). Ancestral-descendant or sister taxon comparisons (Categories 3 through 8 in Table S1B) provide the strongest evidence that genetic accommodation is frequent


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in nature: we found 55 studies in these categories in our survey, representing 37 different species of vertebrates, arthropods, and plants. An additional 46 studies fall into the next strongest support categories (experimental evolution 11–16, and phylogenetic inference 19–24). In addition to further documenting the form and prevalence of phenotypic and genetic accommodation, the ripest areas for future research involve understanding how accommodation of some traits alters selection on other aspects of the phenotype, producing adaptively integrated organisms. Furthermore, while mechanisms of plasticity are becoming better understood, more work needs to be done to uncover the genetic and epigenetic bases for genetic accommodation. Key questions include whether there are genetic signatures of accommodation, whether particular forms of plasticity or epigenetic marking are more readily accommodated, and whether the specific nature of genetic or epigenetic architecture constrains evolutionary outcomes. In addition, insights into how responses to external signals evolve will likely inform our understanding of the evolution of developmental processes in general. Although many systems can reveal individual pieces of a larger puzzle, the gold standard is, for a single system, to understand the complete set of links between environmental variation, developmental responses, and changes to genetic and epigenetic architecture over the course of evolution. Several outstanding natural and experimental examples have documented both patterns and mechanisms (Lee 1999; Suzuki and Nijhout 2006, 2008a, b; Scoville and Pfrender 2010; Lee et al. 2011; Rohner et al. 2013), and as genomic tools become ever more accessible, we anticipate that this list of exemplars will grow rapidly. Many well-studied model and, increasingly, nonmodel systems with phylogenies and population genealogies allow in-depth examination of evolutionary trajectories of populations, ecotypes, and sister species in nature (ants and other social insects, Daphnia, sticklebacks— Gasterosteus, the butterfly Bicyclus, the plant genera Arabidopsis and Mimulus, house finches—Carpodacus, the salmonids Coregonus and Salvelinus, the copepods Eurytemora and Tigriopus, guppies and other poeciliids, and many others—see also Renn and Schumer 2013). Growing attention is also being paid to the advantages provided by resurrection studies (Franks and Hoffmann 2012; Shaw and Etterson 2012). In addition, there will certainly be no shortage of range expansions of species, either “natural” or due to introductions, that will be prime candidates for studies of the role of plasticity in adaptation to global change, as well as how it evolves over short time spans. Finally, experimental evolution of short-generation taxa will continue to play a fundamental role for documenting evolutionary time courses and ascertaining mechanistic details. And these details, whether from experimental evolution or natural systems will be vital for understanding the relative roles of evolution of genetic and epigenetic factors in the control of plastic responses.

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The perspective of evolution via genetic accommodation enhances our understanding of evolution beyond what a reliance on the evolution from standing genetic variation can provide. Imagining phenotypic plasticity or epigenetic modification as an initiator of evolutionary change yields additional insights into questions as diverse as how populations cope with rapidly changing environments, how populations can cross low fitness “valleys,” and what is the “origin” of novel phenotypes. As natural populations face unprecedented rates of environmental change, understanding the interaction between developmental and evolutionary responses is paramount if we are to predict which species are most likely to cope, which are most likely to become pests, and which are most vulnerable to extinction.

ACKNOWLEDGMENTS The authors thank K. Donohue for the opportunity and stimulus to take a rigorous look at the evidence and for her insightful editing. CDS acknowledges support from NSF DEB-Dimensions of Biodiversity 1046328.

LITERATURE CITED Adams, C. E., and F. A. Huntingford. 2002. The functional significance of inherited differences in feeding morphology in a sympatric polymorphic population of Arctic charr. Evol. Ecol. 16:15–25. Alkorta-Aranburu, G., C. M. Beall, D. B. Witonsky, A. Gebremedhin, J. K. Pritchard, and A. Di Rienzo. 2012. The genetic architecture of adaptations to high altitude in Ethiopia. PLoS Genet. 8:e1003110. Ancel, L. W. 2000. Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor. Popul. Biol. 58:307–319. Angers, B., E. Castonguay, and R. Massicotte. 2010. Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol. Ecol. 19:1283–1295. Arnqvist, G., and F. Johansson. 1998. Ontogenetic reaction norms of predatorinduced defensive morphology in dragonfly larvae. Ecology 79:1847– 1858. Aubin-Horth, N., and S. C. P. Renn. 2009. Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol. Ecol. 18:3763–3780. Aubret, F. 2004. Aquatic locomotion and behaviour in two disjunct populations of Western Australian tiger snakes, Notechis ater occidentalis. Aust. J. Zool. 52:357–368. Aubret, F., and R. Shine. 2009. Genetic assimilation and the postcolonization erosion of phenotypic plasticity in island tiger snakes. Curr. Biol. 19:1932–1936. ———. 2010. Fitness costs may explain the post-colonisation erosion of phenotypic plasticity. J. Exp. Biol. 213:735–739. Badyaev, A. V. 2005. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc. R. Soc. Lond. B 272:877–886. ———. 2009. Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philos. Trans. R. Soc. Lond. B 364:1125–1141. Badyaev, A. V., and K. R. Foresman. 2000. Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proc. R. Soc. Lond. Ser. B 267:371–378. Baldwin, J. M. 1896a. A new factor in evolution. Am. Nat. 30:441–451. ———. 1896b. A new factor in evolution (continued). Am. Nat. 30:536–553.

SPECIAL SECTION

Bateman, K. G. 1959. The genetic assimilation of the dumpy phenocopy. J. Genet. 56:341–351. Bateson, P. 1988. The active role of behaviour in evolution. Pp. 191–207 in M.-W. Ho and S. Fox, eds. Process and metaphors in evolution. Wiley, Chichester, U.K. Baythavong, B. S., and M. L. Stanton. 2010. Characterizing selection on phenotypic plasticity in response to natural environmental heterogeneity. Evolution 64:2904–2920. Beall, C. M. 2006. Andean, Tibetan, and Ethiopian patterns of adaptation to high-altitude hypoxia. Integr. Comp. Biol. 46:18–24. Beall, C. M., M. J. Decker, G. M. Brittenham, I. Kushner, A. Gebremedhin, and K. P. Strohl. 2002. An Ethiopian pattern of human adaptation to high-altitude hypoxia. Proc. Natl. Acad. Sci. USA 99:17215–17218. Becker, C., J. Hagmann, J. Müller, D. Koenig, O. Stegle, K. Borgwardt, and D. Weigel. 2011. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:245–249. Beldade, P., A. R. A. Mateus, and R. A. Keller. 2011. Evolution and molecular mechanisms of adaptive developmental plasticity. Mol. Ecol. 20:1347– 1363. Bell, M. A., and S. A. Foster. 1994. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, New York. Bell, M. A., W. E. Aguirre, and N. J. Buck. 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824. Bento, G., A. Ogawa, and R. J. Sommer. 2010. Co-option of the hormonesignalling module dafachronic acid-DAF-12 in nematode evolution. Nature 466:494–497. Berger, S. L., T. Kouzarides, R. Shiekhattar, and A. Shilatifard. 2009. An operational definition of epigenetics. Genes Dev. 23:781–783. Bigham, A. W., M. Bauchet, D. Pinto, X. Mao, J. M. Akey, R. Mei, S. W. Scherer, C. G. Julian, M. J. Wilson, D. L. Herráez, et al. 2010. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 6:e1001116. Bonasio, R., S. J. Tu, and D. Reinberg. 2010. Molecular signals of epigenetic states. Science 330:612–616. Bonduriansky, R., and T. Day. 2009. Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40:103–125. Bossdorf, O., D. Arcuri, C. L. Richards, and M. Pigliucci. 2010. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol. Ecol. 24:541– 553. Braendle, C., and T. Flatt. 2006. A role for genetic accommodation in evolution? Bioessays 28:868–873. Brautigam, K., K. J. Vining, C. Lafon-Placette, C. G. Fossdal, M. Mirouze, J. G. Marcos, S. Fluch, M. F. Fraga, M. A. Guevara, D. Abarca, et al. 2013. Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol. Evol. 3:399–415. Candolin, U. 2009. Population responses to anthropogenic disturbance: lessons from three-spined sticklebacks Gasterosteus aculeatus in eutrophic habitats. J. Fish Biol. 75:2108–2121. Chapman, R. W., A. Mancia, M. Beal, A. Veloso, C. Rathburn, A. Blair, A. F. Holland, G. W. Warr, G. Didinato, I. M. Sokolova, et al. 2011. The transcriptomic responses of the eastern oyster, Crassostrea virginica, to environmental conditions. Mol. Ecol. 20:1431–1449. Chen, F., W. Zhang, Y. Liang, J. L. Huang, K. Li, C. D. Green, J. C. Liu, G. J. Zhang, B. Zhou, X. Yi, et al. 2012a. Transcriptome and network changes in climbers at extreme altitudes. PLoS One 7:e31645. Chen, L. G., Y. Song, S. J. Li, L. P. Zhang, C. S. Zou, and D. Q. Yu. 2012b. The role of WRKY transcription factors in plant abiotic stresses. Biochim. Biophys. Acta. 1819:120–128.

Chevin, L.-M., and R. Lande. 2010. When do adaptive plasticity and genetic evolution prevent extinction of a density-regulated population? Evolution 64:1143–1150. ———. 2011. Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J. Evol. Biol. 24:1462–1476. Chevin, L.-M., R. Lande, and G. M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8:e1000357. Cheviron, Z. A., A. Whitehead, and R. T. Brumfield. 2008. Transcriptomic variation and plasticity in rufous-collared sparrows (Zonotrichia capensis) along an altitudinal gradient. Mol. Ecol. 17:4556–4569. Colbourne, J. K., M. E. Pfrender, D. Gilbert, W. K. Thomas, A. Tucker, T. H. Oakley, S. Tokishita, A. Aerts, G. J. Arnold, M. K. Basu, et al. 2011. The ecoresponsive genome of Daphnia pulex. Science 331:555– 561. Conover, D. O., T. A. Duffy, and L. A. Hice. 2009. The covariance between genetic and environmental influences across ecological gradients: reassessing the evolutionary significance of countergradient and cogradient variation. Ann. N. Y. Acad. Sci. 1168:100–129. Conover, D. O., and E. T. Schultz. 1995. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol. Evol. 10:248–252. Contreras-Cubas, C., M. Palomar, M. Arteaga-Vazquez, J. Luis Reyes, and A. A. Covarrubias. 2012. Non-coding RNAs in the plant response to abiotic stress. Planta 236:943–958. Cooley, J. R., C. Simon, D. C. Marshall, K. Slon, and C. Ehrhardt. 2001. Allochronic speciation, secondary contact, and reproductive character displacement in periodical cicadas (Hemiptera: Magicicada spp.): genetic, morphological, and behavioural evidence. Mol. Ecol. 10:661– 671. Coolon, J. D., K. L. Jones, T. C. Todd, B. C. Carr, and M. A. Herman. 2009. Genomic response to soil bacteria predicts environment-specific genetic effects on life history traits. PLoS Genet. 5:e1000503. Crispo, E. 2007. The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479. Czesak, M. E., and C. W. Fox. 2003. Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments. Evolution 57:1121–1132. Day, T., and R. Bonduriansky. 2011. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178:E18– E36. Debat, V., A. Debelle, and I. Dworkin. 2009. Plasticity, canalization, and developmental stability of the Drosophila wing: joint effects of mutations and developmental temperature. Evolution 63:2864–2876. Deere, K. A., G. F. Grether, A. Sun, and J. S. Sinsheimer. 2012. Female mate preference explains countergradient variation in the sexual coloration of guppies (Poecilia reticulata). Proc. R. Soc. Lond. B 279:1684–1690. Dennis, S. R., M. J. Carter, W. T. Hentley, and A. P. Beckerman. 2011. Phenotypic convergence along a gradient of predation risk. Proc. R. Soc. Lond. B 278:1687–1696. Dickins, T. E., and Q. Rahman. 2012. The extended evolutionary synthesis and the role of soft inheritance in evolution. Proc. R. Soc. Lond. B 279:2913–2921. Donovan, L. A., and J. R. Ehleringer. 1994. Potential for selection on plants for water-use efficiency as estimated by carbon isotope discrimination. Am. J. Bot. 81:927–935. Draghi, J. A., and M. C. Whitlock. 2012. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66:2891–2902.


667

SPECIAL SECTION

Dun, R. B., and A. S. Fraser. 1959. Selection for an invariant character, vibrissa number, in the house mouse. Aust. J. Biol. Sci. 12:506–523. DuRant, S. E., W. K. Hopkins, G. R. Hepp, and J. R. Walters. 2013. Ecological, evolutionary, and conservation implications of incubation temperaturedependent phenotypes in birds. Biol. Rev. 88:499–509. Dworkin, I. 2005a. Canalization, cryptic variation and developmental buffering: a critical examination and analytical perspective. Pp. 131–158 in B. Hallgrimsson and B. K. Hall, eds. Variation: a central concept in biology. Academic Press, New York. ———. 2005b. A study of canalization and developmental stability in the sternopleural bristle system of Drosophila melanogaster. Evolution 59:1500–1509. Eldar, A., V. K. Chary, P. Xenopoulos, M. E. Fontes, O. C. Loson, J. Dworkin, P. J. Piggot, and M. B. Elowitz. 2009. Partial penetrance facilitates developmental evolution in bacteria. Nature 460:510–514. Engqvist, L. 2007. Environment-dependent genetic correlations between development time and body mass in a scorpionfly. Zoology 110:344–353. Falconer, D. S. 1990. Selection in different environments: effects on environmental sensitivity (reaction norm) and on mean performance. Genet. Res. 56:57–70. Faulk, C., and D. C. Dolinoy. 2011. Timing is everything: The when and how of environmentally induced changes in the epigenome of animals. Epigenetics 6:791–797. Feinberg, A. P., and R. A. Irizarry. 2010. Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc. Natl. Acad. Sci. USA 107:1757–1764. Félix, M.-A., and A. Wagner. 2008. Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity 100:132–140. Fitzpatrick, B. M. 2012. Underappreciated consequences of phenotypic plasticity for ecological speciation. Int. J. Ecol. 2012:256017. Flatt, T. 2005. The evolutionary genetics of canalization. Q. Rev. Biol. 80:287– 316. Flores, K. B., F. Wolschin, and G. V. Amdam. 2013. The role of methylation of DNA in environmental adaptation. Integr. Comp. Biol. 53:359– 372. Frank, S. A. 2011. Natural selection. II. Developmental variability and evolutionary rate. J. Evol. Biol. 24:2310–2320. Franks, S. J., and A. A. Hoffmann. 2012. Genetics of climate change adaptation. Annu. Rev. Genet. 46:185–208. Furrow, R., and M. W. Feldman. 2014. Genetic variation, environmental variability, and the evolution of epigenetic regulation. Evolution 68:673–683. Gasch, A. P., P. T. Spellman, C. M. Kao, O. Carmel-Harel, M. B. Eisen, G. Storz, D. Botstein, and P. O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241–4257. Ge, R. L., T. S. Simonson, R. C. Cooksey, U. Tanna, G. Qin, C. D. Huff, D. J. Witherspoon, J. C. Xing, Z. Z. Bai, J. T. Prchal, et al. 2012. Metabolic insight into mechanisms of high-altitude adaptation in Tibetans. Mol. Genet. Metab. 106:244–247. Gelmond, O., F. A. von Hippel, and M. S. Christy. 2009. Rapid ecological speciation in three-spined stickleback Gasterosteus aculeatus from Middleton Island, Alaska: the roles of selection and geographic isolation. J. Fish Biol. 75:2037–2051. Geoghegan, J. L., and H. G. Spencer. 2012. Population-epigenetic models of selection. Theor. Popul. Biol. 81:232–242. Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N. Reznick. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21:394–407.

668


Gibert, J. M., F. Peronnet, and C. Schlotterer. 2007. Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet. 3:266–280. Gibson, G., and I. Dworkin. 2004. Uncovering cryptic genetic variation. Nat. Rev. Genet. 5:681–690. Gibson, G., and D. S. Hogness. 1996. Effect of polymorphism in the Drosophila regulatory gene ultrabithorax on homeotic stability. Science 271:200–203. Gilbert, S. F., and D. Epel. 2009. Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer Associates, Sunderland, MA. Godoy, O., A. Saldana, N. Fuentes, F. Valladares, and E. Gianoli. 2011. Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biol. Invasions 13:1615–1625. Gomez-Mestre, I., and D. R. Buchholz. 2006. Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc. Natl. Acad. Sci. USA 103:19021–19026. Gorur, G., C. Lomonaco, and A. Mackenzie. 2005. Phenotypic plasticity in host-plant specialisation in Aphis fabae. Ecol. Entomol. 30:657–664. Gracey, A. Y., E. J. Fraser, W. Li, Y. Fang, R. R. Taylor, J. Rogers, A. Brass, and A. R. Cossins. 2004. Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl. Acad. Sci. USA 101:16970–16975. Grativol, C., A. S. Hemerly, and P. C. G. Ferreira. 2012. Genetic and epigenetic regulation of stress responses in natural plant populations. Biochim. Biophys. Acta 1819:176–185. Grether, G. F. 2005. Environmental change, phenotypic plasticity, and genetic compensation. Am. Nat. 166:E115–E123. Grether, G. F. 2013. Redesigning the genetic architecture of phenotypically plastic traits in a changing environment. Biol. J. Linn. Soc. doi: 10.1111/bij.12064. Grether, G. F., M. E. Cummings, and J. Hudon. 2005. Countergradient variation in the sexual coloration of guppies (Poecilia reticulata): drosopterin synthesis balances carotenoid availability. Evolution 59:175–188. Hairston, N. G., and L. De Meester. 2008. Daphnia paleogenetics and environmental change: deconstructing the evolution of plasticity. Int. Rev. Hydrobiol. 93:578–592. Harvey, A. W. 1998. Genes for asymmetry easily overruled. Nature 392:345– 346. Haugen, R., L. Steffes, J. Wolf, P. Brown, S. Matzner, and D. H. Siemens. 2008. Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching. Oikos 117:231–244. Hendry, A. P., T. F. Farrugia, and M. T. Kinnison. 2008. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol. 17:20–29. Herman, J. J., H. G. Spencer, K. Donohue, and S. E. Sultan. 2014. How stable “should” epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution 68: 632–643. Hermisson, J., and G. P. Wagner. 2004. The population genetic theory of hidden variation and genetic robustness. Genetics 168:2271–2284. Herrera, C. M., and P. Bazaga. 2013. Epigenetic correlates of plant phenotypic plasticity: DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees. Bot. J. Linn. Soc. 171:441–452. Herrera, C. M., M. I. Pozo, and P. Bazaga. 2012. Jack of all nectars, master of most: DNA methylation and the epigenetic basis of niche width in a flower-living yeast. Mol. Ecol. 21:2602–2616. Hinton, G. E., and S. J. Nowlan. 1987. How learning can guide evolution. Complex Syst. 1:495–502.

SPECIAL SECTION

Hodgins, K. A., and L. H. Rieseberg. 2011. Genetic differentiation in lifehistory traits of introduced and native common ragweed (Ambrosia artemisiifolia) populations. J. Evol. Biol. 24:2731–2749. Hodgins, K. A., Z. Lai, K. Nurkowski, J. Huang, and L. H. Rieseberg. 2013. The molecular basis of invasiveness: differences in gene expression of native and introduced common ragweed (Ambrosia artemisiifolia) in stressful and benign environments. Mol. Ecol. 22:2496– 2510. Hodgins-Davis, A., and J. P. Townsend. 2009. Evolving gene expression: from G to E to G×E. Trends Ecol. Evol. 24:649–665. Holeski, L. M. 2007. Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. J. Evol. Biol. 20:2092–2100. Holeski, L. M., G. Jander, and A. A. Agrawal. 2012. Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol. Evol. 27:618–626. Huerta-Sanchez, E., M. DeGiorgio, L. Pagani, A. Tarekegn, R. Ekong, T. Antao, A. Cardona, H. E. Montgomery, G. L. Cavalleri, P. A. Robbins, et al. 2013. Genetic signatures reveal high-altitude adaptation in a set of Ethiopian populations. Mol. Biol. Evol. 30:1877–1888. Hunt, B. G., L. Ometto, L. Keller, and M. A. D. Goodisman. 2013. Evolution at two levels in fire ants: the relationship between patterns of gene expression and protein sequence evolution. Mol. Biol. Evol. 30:263– 271. Iwasaki, W. M., M. E. Tsuda, and M. Kawata. 2013. Genetic and environmental factors affecting cryptic variations in gene regulatory networks. BMC Evol. Biol. 13:91. Jablonka, E. 2013. Epigenetic inheritance and plasticity: the responsive germline. Prog. Biophys. Mol. Biol. 111:99–107. Jablonka, E., and M. J. Lamb. 1995. Epigenetic inheritance and evolution: the Lamarckian dimension. Oxford Univ. Press, Oxford, U.K. ———. 1998. Epigenetic inheritance in evolution. J. Evol. Biol. 11:159–183. ———. 2005. Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge, MA. Jablonka, E., and G. Raz. 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84:131–176. Janzen, F. J., and G. L. Paukstis. 1991. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66:149–179. Johannes, F., E. Porcher, F. K. Teixeira, V. Saliba-Colombani, M. Simon, N. Agier, A. Bulski, J. Albuisson, F. Heredia, P. Audigier, et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5:e1000530. Johnson, L. J., and P. J. Tricker. 2010. Epigenomic plasticity within populations: its evolutionary significance and potential. Heredity 105:113–121. Juenger, T., T. Lennartsson, and J. Tuomi. 2000. The evolution of tolerance to damage in Gentianella campestris: natural selection and the quantitative genetics of tolerance. Evol. Ecol. 14:393–419. Kalisz, S., and M. D. Purugganan. 2004. Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol. Evol. 19:309–314. Keith, B., R. S. Johnson, and M. C. Simon. 2012. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 12:9–22. Khraiwesh, B., J. K. Zhu, and J. H. Zhu. 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta 1819:137–148. Kilian, J., F. Peschke, K. W. Berendzen, K. Harter, and D. Wanke. 2012. Prerequisites, performance and profits of transcriptional profiling the abiotic stress response. Biochim. Biophys. Acta 1819:166–175.

King, E. G., D. A. Roff, and D. J. Fairbairn. 2011. The evolutionary genetics of acquisition and allocation in the wing dimorphic cricket, Gryllus firmus. Evolution 65:2273–2285. Klironomos, F. D., J. Berg, and S. Collins. 2013. How epigenetic mutations can affect genetic evolution: model and mechanism. Bioessays 35:571–578. Lahti, D. C., N. A. Johnson, B. C. Ajie, S. P. Otto, A. P. Hendry, D. T. Blumstein, R. G. Coss, K. Donohue, and S. A. Foster. 2009. Relaxed selection in the wild. Trends Ecol. Evol. 24:487–496. Lande, R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22:1435– 1446. Larsen, P. F., E. E. Nielsen, T. D. Williams, and V. Loeschcke. 2008. Intraspecific variation in expression of candidate genes for osmoregulation, heme biosynthesis and stress resistance suggests local adaptation in European flounder (Platichthys flesus). Heredity 101:247–259. ¨ Carlborg. 2008. Evolutionary potential of hidden genetic Le Rouzic, A., and O. variation. Trends Ecol. Evol. 23:33–37. Le Trionnaire, G., S. Jaubert-Possamai, J. Bonhomme, J.-P. Gauthier, G. Guernec, A. Le Cam, F. Legeai, J. Monfort, and D. Tagu. 2012. Transcriptomic profiling of the reproductive mode switch in the pea aphid in response to natural autumnal photoperiod. J. Insect Physiol. 58:1517– 1524. Ledon-Rettig, C. C., D. W. Pfennig, and E. J. Crespi. 2010. Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies. Proc. R. Soc. Lond. B 277:3569–3578. Lee, C. E. 1999. Rapid and repeated invasions of fresh water by the copepod Eurytemora affinis. Evolution 53:1423–1434. Lee, C. E., M. Kiergaard, G. W. Gelembiuk, B. D. Eads, and M. Posavi. 2011. Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evolution 65:2229–2244. Lee, C. E., and C. H. Petersen. 2002. Genotype-by-environment interaction for salinity tolerance in the freshwater-invading copepod Eurytemora affinis. Physiol. Biochem. Zool. 75:335–344. Levin, D. A. 2009. Flowering-time plasticity facilitates niche shifts in adjacent populations. New Phytol. 183:661–666. Lindquist, S. 2009. Protein folding sculpting evolutionary change. Cold Spring Harb. Symp. Quant. Biol. 74:103–108. Luo, M., X. C. Liu, P. Singh, Y. H. Cui, L. Zimmerli, and K. Q. Wu. 2012. Chromatin modifications and remodeling in plant abiotic stress responses. Biochim. Biophys. Acta 1819:129–136. Macke, E., S. Magalhães, F. Bach, and I. Olivieri. 2011. Experimental evolution of reduced sex ratio adjustment under local mate competition. Science 334:1127–1129. Masel, J., and M. V. Trotter. 2010. Robustness and evolvability. Trends Genet. 26:406–414. Massicotte, R., and B. Angers. 2012. General-purpose genotype or how epigenetics extend the flexibility of a genotype. Genet. Res. Int. 2012: 317175. Mather, K. 1942. Polygenic inheritance and natural selection. Biol. Rev. 18:32–64. Maughan, H., C. W. Birky, and W. L. Nicholson. 2009. Transcriptome divergence and the loss of plasticity in Bacillus subtilis after 6,000 generations of evolution under relaxed selection for sporulation. J. Bacteriol. 191:428–433. Mayr, E. 1958. Behavior and systematics. Pp. 341–362 in A. Roe and G. G. Simpson, eds. Behavior and evolution. Yale Univ. Press, New Haven, CT. ———. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA. McCairns, R. J. S., and L. Bernatchez. 2010. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic


669

SPECIAL SECTION

plasticity from an integrated analysis of candidate gene expression. Evolution 64:1029–1047. McGuigan, K., N. Nishimura, M. Currey, D. Hurwit, and W. A. Cresko. 2011. Cryptic genetic variation and body size evolution in threespine stickleback. Evolution 65:1203–1211. McGuigan, K., and C. M. Sgrò. 2009. Evolutionary consequences of cryptic genetic variation. Trends Ecol. Evol. 24:305–311. Messina, F. J., and J. D. Fry. 2003. Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. J. Evol. Biol. 16:501–509. Miner, B. G., S. E. Sultan, S. G. Morgan, D. K. Padilla, and R. A. Relyea. 2005. Ecological consequences of phenotypic plasticity. Trends Ecol. Evol. 20:685–692. Mishra, P. K., M. Baum, and J. Carbon. 2011. DNA methylation regulates phenotype-dependent transcriptional activity in Candida albicans. Proc. Natl. Acad. Sci. USA 108:11965–11970. Mizoi, J., K. Shinozaki, and K. Yamaguchi-Shinozaki. 2012. AP2/ERF family transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819:86–96. Moczek, A. P. 2007. Developmental capacitance, genetic accommodation, and adaptive evolution. Evol. Dev. 9:299–305. Moczek, A. P., S. Sultan, S. Foster, C. Ledon-Rettig, I. Dworkin, H. F. Nijhout, E. Abouheif, and D. W. Pfennig. 2011. The role of developmental plasticity in evolutionary innovation. Proc. R. Soc. Lond. B 278:2705– 2713. Morgan, C. L. 1896. On modification and variation. Science 4:733–740. Muller, H. J. 1949. Reintegration of the symposium on genetics, paleontology and evolution. In G. Jepsen, G. G. Simpson, and E. Mayr, eds. Genetics, paleontology and evolution. Princeton Univ. Press, Princeton, NJ. Nakashima, K., H. Takasaki, J. Mizoi, K. Shinozaki, and K. YamaguchiShinozaki. 2012. NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819:97–103. Nespolo, R. F., F. Halkett, C. C. Figueroa, M. Plantegenest, and J. C. Simon. 2009. Evolution of trade-offs between sexual and asexual phases and the role of reproductive plasticity in the genetic architecture of aphid life histories. Evolution 63:2402–2412. Osakabe, Y., K. Yamaguchi-Shinozaki, K. Shinozaki, and L. S. P. Tran. 2013. Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J. Exp. Bot. 64:445–458. Osborn, H. F. 1897. Organic selection. Science 6:583–587. Otaki, J. M., A. Hiyama, M. Iwata, and T. Kudo. 2010. Phenotypic plasticity in the range-margin population of the lycaenid butterfly Zizeeria maha. BMC Evol. Biol. 10:252. Paenke, I., B. Sendhoff, and T. J. Kawecki. 2007. Influence of plasticity and learning on evolution under directional selection. Am. Nat. 170:E47– E58. Pfennig, D. W., and M. McGee. 2010. Resource polyphenism increases species richness: a test of the hypothesis. Philos. Trans. R. Soc. Lond. B 365:577– 591. Pfennig, D. W., M. A. Wund, E. C. Snell-Rood, T. Cruickshank, C. D. Schlichting, and A. P. Moczek. 2010. Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol. Evol. 25:459–467. Pigliucci, M., and C. J. Murren. 2003. Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57:1455–1464. Pigliucci, M., C. J. Murren, and C. D. Schlichting. 2006. Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 209:2362–2367. Price, T. D., A. Qvarnstrom, and D. E. Irwin. 2003. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B 270:1433– 1440.

670


Price, T. D., P. J. Yeh, and B. Harr. 2008. Phenotypic plasticity and the evolution of a socially selected trait following colonization of a novel environment. Am. Nat. 172:S49–S62. Puranik, S., P. P. Sahu, P. S. Srivastava, and M. Prasad. 2012. NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 17:369–381. Queitsch, C., T. A. Sangster, and S. L. Lindquist. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624. Rabbani, M. A., K. Maruyama, H. Abe, M. A. Khan, K. Katsura, Y. Ito, K. Yoshiwara, M. Seki, K. Shinozaki, and K. Yamaguchi-Shinozaki. 2003. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol. 133:1755– 1767. Rajakumar, R., D. San Mauro, M. B. Dijkstra, M. H. Huang, D. E. Wheeler, F. Hiou-Tim, A. Khila, M. Cournoyea, and E. Abouheif. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335:79–82. Rapp, R. A., and J. F. Wendel. 2005. Epigenetics and plant evolution. New Phytol. 168:81–91. Rasmann, S., M. de Vos, C. L. Casteel, D. Tian, R. Halitschte, J. Y. Sun, A. A. Agrawal, G. W. Felton, and G. Jander. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 158:854–863. Reale, D., D. Berteaux, A. G. McAdam, and S. Boutin. 2003. Lifetime selection on heritable life-history traits in a natural population of red squirrels. Evolution 57:2416–2423. Renn, S. C. P., and M. E. Schumer. 2013. Genetic accommodation and behavioural evolution: insights from genomic studies. Anim. Behav. 85:1012–1022. Richards, C. L., O. Bossdorf, and M. Pigliucci. 2010. What role does heritable epigenetic variation play in phenotypic evolution? BioScience 60:232– 237. Richards, C. L., A. W. Schrey, and M. Pigliucci. 2012. Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol. Lett. 15:1016–1025. Robertson, F. W. 1964. The ecological genetics of growth in Drosophila. 7. The role of canalization in the stability of growth relations. Genet. Res. 5:107–126. Robinson, B. W., and R. Dukas. 1999. The influence of phenotypic modifications on evolution: the Baldwin effect and modern perspectives. Oikos 85:582–589. Robinson, M. R., A. J. Wilson, J. G. Pilkington, T. H. Clutton-Brock, J. M. Pemberton, and L. E. B. Kruuk. 2009. The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep. Genetics 181:1639–1648. Roelofs, D., J. Morgan, and S. Sturzenbaum. 2010. The significance of genome-wide transcriptional regulation in the evolution of stress tolerance. Evol. Ecol. 24:527–539. Rohner, N., D. F. Jarosz, J. E. Kowalko, M. Yoshizawa, W. R. Jeffery, R. L. Borowsky, S. L. Lindquist, and C. J. Tabin. 2013. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342:1372–1375. Rollo, C. D. 1994. Phenotypes: their epigenetics, ecology and evolution. Chapman and Hall, London. Rossiter, M. C. 1996. Incidence and consequences of inherited environmental effects. Annu. Rev. Ecol. Syst. 27:451–476. Ruden, D. M. 2011. The (new) new synthesis and epigenetic capacitors of morphological evolution. Nat. Genet. 43:88–89. Rutherford, S. L., and S. Lindquist. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336–342.

SPECIAL SECTION

Saito, N., S. Ishihara, and K. Kaneko. 2013. Baldwin effect under multipeaked fitness landscapes: phenotypic fluctuation accelerates evolutionary rate. Phys. Rev. E 87:052701. Sangster, T. A., N. Salathia, S. Undurraga, R. Milo, K. Schellenberg, S. Lindquist, and C. Queitsch. 2008. HSP90 affects the expression of genetic variation and developmental stability in quantitative traits. Proc. Natl. Acad. Sci. USA 105:2963–2968. Savolainen, V., M.-C. Anstett, C. Lexer, I. Hutton, J. J. Clarkson, M. V. Norup, M. P. Powell, D. Springate, N. Salamin, and W. J. Baker. 2006. Sympatric speciation in palms on an oceanic island. Nature 441:210–213. Scharf, K. D., T. Berberich, I. Ebersberger, and L. Nover. 2012. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 1819:104–119. Scheinfeldt, L. B., S. Soi, S. Thompson, A. Ranciaro, D. Woldemeskel, W. Beggs, C. Lambert, J. P. Jarvis, D. Abate, G. Belay, et al. 2012. Genetic adaptation to high altitude in the Ethiopian highlands. Genome Biol. 13:R1. Schlichting, C. D. 2004. The role of phenotypic plasticity in diversification. Pp. 191–200 in T. J. DeWitt and S. M. Scheiner, eds. Phenotypic plasticity: functional and conceptual approaches. Oxford Univ. Press, Oxford, U.K. ———. 2008. Hidden reaction norms, cryptic variation and evolvability. Ann. N. Y. Acad. Sci. 1133:187–203. Schlichting, C. D., and M. Pigliucci. 1998. Phenotypic evolution: a reaction norm perspective. Sinauer Associates, Sunderland, MA. Schlichting, C. D., and H. Smith. 2002. Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes. Evol. Ecol. 16:189–211. Schmalhausen, I. I. 1949. Factors of evolution. Blakiston, Philadelphia, PA. Schmitz, R. J., M. D. Schultz, M. G. Lewsey, R. C. O’Malley, M. A. Urich, O. Libiger, N. J. Schork, and J. R. Ecker. 2011. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369–373. Schwartz, C., S. Balasubramanian, N. Warthmann, T. P. Michael, J. Lempe, S. Sureshkumar, Y. Kobayashi, J. N. Maloof, J. O. Borevitz, J. Chory, et al. 2009. Cis-regulatory changes at FLOWERING LOCUS T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183:723–732. Scoville, A. G., L. L. Barnett, S. Bodbyl-Roels, J. K. Kelly, and L. C. Hileman. 2011. Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol. 191:251–263. Scoville, A. G., and M. Pfrender. 2010. Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl. Acad. Sci. USA 107:4260–4263. Shaw, K. A., M. L. Scotti, and S. A. Foster. 2007. Ancestral plasticity and the evolutionary diversification of courtship behaviour in threespine sticklebacks. Anim. Behav. 73:415–422. Shaw, R. G., and J. R. Etterson. 2012. Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics. New Phytol. 195:752–765. Shea, N., I. Pen, and T. Uller. 2011. Three epigenetic information channels and their different roles in evolution. J. Evol. Biol. 24:1178–1187. Sherrard, M. E., H. Maherali, and R. G. Latta. 2009. Water stress alters the genetic architecture of functional traits associated with drought adaptation in Avena barbata. Evolution 63:702–715. Simonson, T. S., Y. Yang, C. D. Huff, H. Yun, G. Qin, D. J. Witherspoon, Z. Bai, F. R. Lorenzo, J. Xing, L. B. Jorde, et al. 2010. Genetic evidence for high-altitude adaptation in Tibet. Science 329:72–75. Smith, C. R., N. S. Mutti, W. C. Jasper, A. Naidu, C. D. Smith, and J. Gadau. 2012. Patterns of DNA methylation in development, division of labor and hybridization in an ant with genetic caste determination. PLoS One 7:e42433.

Smith, G., and M. G. Ritchie. 2013. How might epigenetics contribute to ecological speciation? Curr. Zool. 59:686–696. Snell-Rood, E. C., J. D. Van Dyken, T. Cruickshank, M. J. Wade, and A. P. Moczek. 2010. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81. Spanier, K. I., F. Leese, C. Mayer, J. K. Colbourne, D. Gilbert, M. E. Pfrender, and R. Tollrian. 2010. Predator-induced defences in Daphnia pulex: selection and evaluation of internal reference genes for gene expression studies with real-time PCR. BMC Mol. Biol. 11:50. Spoljaric, M. A., and T. E. Reimchen. 2011. Habitat-specific trends in ontogeny of body shape in stickleback from coastal archipelago: potential for rapid shifts in colonizing populations. J. Morphol. 272:590–597. Springate, D. A., N. Scarcelli, J. Rowntree, and P. X. Kover. 2011. Correlated response in plasticity to selection for early flowering in Arabidopsis thaliana. J. Evol. Biol. 24:2280–2288. Stasiuk, S. J., M. J. Scott, and W. N. Grant. 2012. Developmental plasticity and the evolution of parasitism in an unusual nematode, Parastrongyloides trichosuri. EvoDevo 3:1. Sultan, S. E. 1995. Phenotypic plasticity and plant adaptation. Acta Bot. Neerl. 44:363–383. Sultan, S. E., K. Barton, and A. M. Wilczek. 2009. Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90:1831–1839. Sultan, S. E., T. Horgan-Kobelski, L. M. Nichols, C. E. Riggs, and R. K. Waples. 2013. A resurrection study reveals rapid adaptive evolution within populations of an invasive plant. Evol. Appl. 6:266–278. Suzuki, Y., and H. F. Nijhout. 2006. Evolution of a polyphenism by genetic accommodation. Science 311:650–652. ———. 2008a. Constraint and developmental dissociation of phenotypic integration in a genetically accommodated trait. Evol. Dev. 10:690–699. ———. 2008b. Genetic basis of adaptive evolution of a polyphenism by genetic accommodation. J. Evol. Biol. 21:57–66. Svanback, R., and D. Schluter. 2012. Niche specialization influences adaptive phenotypic plasticity in the threespine stickleback. Am. Nat. 180:50–59. Sword, G. A. 2002. A role for phenotypic plasticity in the evolution of aposematism. Proc. R. Soc. Lond. Ser. B 1501:1639–1644. Takahashi, K. H. 2013. Multiple capacitors for natural genetic variation in Drosophila melanogaster. Mol. Ecol. 22:1356–1365. Thibert-Plante, X., and A. P. Hendry. 2011. The consequences of phenotypic plasticity for ecological speciation. J. Evol. Biol. 24:326–342. Tine, M., B. Guinand, and J. D. Durand. 2012. Variation in gene expression along a salinity gradient in wild populations of the euryhaline black-chinned tilapia Sarotherodon melanotheron. J. Fish Biol. 80: 801. Tirosh, I., S. Reikhav, N. Sigal, Y. Assia, and N. Barkai. 2010. Chromatin regulators as capacitors of interspecies variations in gene expression. Mol. Syst. Biol. 6:435. Tsang, L. M., T. Y. Chan, S. T. Ahyong, and K. H. Chu. 2011. Hermit to king, or hermit to all: multiple transitions to crab-like forms from hermit crab ancestors. Syst. Biol. 60:616–629. Turck, F., and G. Coupland. 2014. Natural variation in epigenetic gene regulation and its effects on plant developmental traits. Evolution 68:620–631. van Hinsberg, A. 1998. Maternal and ambient environmental effects of light on germination in Plantago lanceolata: correlated responses to selection on leaf length. Funct. Ecol. 12:825–833. van Kleunen, M., and M. Fischer. 2001. Adaptive evolution of plastic foraging responses in a clonal plant. Ecology 82:3309–3319. Waddington, C. H. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563–565.


671

SPECIAL SECTION

———. 1953. Genetic assimilation of an acquired character. Evolution 7:118– 126. ———. 1956. Genetic assimilation of the bithorax phenotype. Evolution 10:1–13. ———. 1957. The strategy of the genes. Allen & Unwin, London. Waterland, R. A., M. Travisano, and K. G. Tahiliani. 2007. Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J. 21:3380–3385. Wcislo, W. T. 1989. Behavioral environments and evolutionary change. Annu. Rev. Ecol. Syst. 20:137–170. Weiner, S. A., and A. L. Toth. 2012. Epigenetics in social insects: a new direction for understanding the evolution of castes. Genet. Res. Int. 2012:609810. West-Eberhard, M. J. 1989. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20:249–278. ———. 2003. Developmental plasticity and evolution. Oxford Univ. Press, New York. ———. 2005a. Developmental plasticity and the origin of species differences. Proc. Natl. Acad. Sci. USA 102:6543–6549. ———. 2005b. Phenotypic accommodation: adaptive innovation due to developmental plasticity. J. Exp. Zool. Part B 304B:610–618. Whitehead, A. 2012. Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation. J. Exp. Biol. 215:884–891. Whitehead, A., J. L. Roach, S. Zhang, and F. Galvez. 2011. Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc. Natl. Acad. Sci. USA 108:6193– 6198. Wolf, J. B., and R. Hager. 2006. A maternal–offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol. 4:e380. Wund, M. A. 2012. Assessing the impacts of phenotypic plasticity on evolution. Integr. Comp. Biol. 52:5–15. Wund, M. A., J. A. Baker, B. Clancy, J. L. Golub, and S. A. Foster. 2008. A test of the “Flexible stem” model of evolution: ancestral plasticity,

genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am. Nat. 172:449–462. Wund, M. A., S. Valena, S. Wood, and J. A. Baker. 2012. Ancestral plasticity and allometry in threespine stickleback reveal phenotypes associated with derived, freshwater ecotypes. Biol. J. Linn. Soc. 105:573– 583. Xiang, K., Ouzhuluobu, Y. Peng, Z. Yang, X.-M. Zhang, C.-Y. Cui, H. Zhang, M. Li, Y.-F. Zhang, Bianba, et al. 2013. Identification of a Tibetanspecific mutation in the hypoxic gene EGLN1 and its contribution to high-altitude adaptation. Mol. Biol. Evol. 30:1889–1898. Xu, S. H., S. L. Li, Y. J. Yang, J. Z. Tan, H. Y. Lou, W. F. Jin, L. Yang, X. D. Pan, J. C. Wang, Y. P. Shen, et al. 2011. A genome-wide search for signals of high-altitude adaptation in Tibetans. Mol. Biol. Evol. 28:1003–1011. Yang, C. Q., X. Fang, X. M. Wu, Y. B. Mao, L. J. Wang, and X. Y. Chen. 2012. Transcriptional regulation of plant secondary metabolism. J. Integr. Plant Biol. 54:703–712. Yant, L. 2012. Genome-wide mapping of transcription factor binding reveals developmental process integration and a fresh look at evolutionary dynamics. Am. J. Bot. 99:277–290. Yeh, P. J., and T. D. Price. 2004. Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am. Nat. 164:531– 542. Yi, X., Y. Liang, E. Huerta-Sanchez, X. Jin, Z. X. P. Cuo, J. E. Pool, X. Xu, H. Jiang, N. Vinckenbosch, T. S. Korneliussen, et al. 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329:75– 78. Zhang, Y.-Y., M. Fischer, V. Colot, and O. Bossdorf. 2013. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197:314–322. Zhou, S. S., T. G. Campbell, E. A. Stone, T. F. C. Mackay, and R. R. H. Anholt. 2012. Phenotypic plasticity of the Drosophila transcriptome. PLoS Genet. 8:e1002593.

Associate Editor: K. Donohue

Supporting Information Additional Supporting Information may be found in the online version of this article at the publisher’s website: Table S1. (A) Role of initial plasticity in stimulating further evolutionary change. (B) Forms of genetic accommodation: plasticity as a facilitator of evolutionary change. Table S2. Studies assigned to different categories of genetic accommodation.

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